pp 1–11 | Cite as

Does range expansion modify trait covariation? A study of a northward expanding dragonfly

  • Allan RaffardEmail author
  • Lieven Therry
  • Fia Finn
  • Kamilla Koch
  • Tomas Brodin
  • Simon Blanchet
  • Julien Cote
Global change ecology – original research


The adaptive value of correlations among phenotypic traits depends on the prevailing environmental conditions. Differences in selection pressures during species range expansions may therefore shape phenotypic integration. In this study, we assessed variation in behavioral and morphological traits, as well as their covariations, in replicated southern and northern European populations of the northward expanding dragonfly Crocothemis erythraea. Larvae from northern populations were, on average, darker in color, and therefore, better camouflaged than larvae from southern populations. However, there was no difference in activity level. Darkness and activity were positively correlated in larvae from northern populations, whereas this trait covariation was missing in southern populations. This suggests the emergence of alternative strategies in time-limited northern populations, a higher activity level that required better camouflage through darker coloration, while less active larvae benefited from an energy-saving strategy by reducing the investment in costly traits, such as body darkness. We further found that larger larvae emerged into larger adults, with a higher investment in flight morphology. Our findings imply that phenotypic integration is associated with the northward range shift, potentially differentially shaping fitness consequences, and ecological interactions in southern versus northern populations.


Behavior Climate change Colonization Growth–predation trade-off Phenotypic architecture Range expansion 



We kindly thank the people that guided us to populations and helped collecting the samples: Yohan Morizet, Philippe Lambret, Charlotte Sohier, Hajnalka Gyulavári, Diana Goertzen and Frank Suhling. ANB-Belgium, Indre Nature, Grand Port Maritime de Marseille and Département Environnement et Aménagement provided permission and access to populations. This study is part of the project PROBIS (Biodiversa) and financially supported by ONEMA, DFG and SEPA. JC is supported by an ANR-12-JSV7-0004-01. JC and SB are part of the Laboratoire d’Excellence (LABEX) entitled TULIP (ANR-10-LABX-41).

Author contribution statement

LT, FF, SB and JC conceived and designed the experiment. LT, FF and KK conducted fieldwork and performed the experiment. LT and AR analyzed the data with input from SB and JC. LT wrote the first draft, AR wrote the revised version and all authors contributed to these versions.

Compliance with ethical standards

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare they have no conflict of interest.

Supplementary material

442_2020_4592_MOESM1_ESM.doc (524 kb)
Supplementary material 1 (DOCX 524 kb)
442_2020_4592_MOESM2_ESM.docx (20 kb)
Supplementary material 2 (DOCX 21 kb)
442_2020_4592_MOESM3_ESM.docx (29 kb)
Supplementary material 3 (DOCX 28 kb)
442_2020_4592_MOESM4_ESM.xls (130 kb)
Supplementary material 4 (XLS 130 kb)
442_2020_4592_MOESM5_ESM.xls (713 kb)
Supplementary material 5 (XLS 713 kb)


  1. Armitage SAO, Siva-Jothy MT (2005) Immune function responds to selection for cuticular colour in Tenebrio molitor. Heredity 94:650–656. CrossRefPubMedGoogle Scholar
  2. Aubret F, Shine R (2009) Genetic assimilation and the postcolonization erosion of phenotypic plasticity in island tiger snakes. Curr Biol 19:1932–1936. CrossRefPubMedGoogle Scholar
  3. Bauhus S (1996) Funde von Crocothemis erythraea (Brullé) und Aeshna affinis (Vanderlinden) in der Lippe-Aue (Anisoptera: Libellulidae, Aeshnidae). Libellula 15:79–84Google Scholar
  4. Beckerman AP, Petchey OL, Morin PJ (2010) Adaptive foragers and community ecology: linking individuals to communities and ecosystems. Funct Ecol 24:1–6. CrossRefGoogle Scholar
  5. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834. CrossRefGoogle Scholar
  6. Benke AC (1970) A method for comparing individual growth rates of aquatic insects with special references to the Odonata. Ecology 51:328–331. CrossRefGoogle Scholar
  7. Bonner JT (2006) Why size matters: from bacteria to blue whales. Princeton Univ. Press., PrincetonGoogle Scholar
  8. Brockaus T, Roland H-J, Benken T et al (2015) Atlas der libellen Deutschlands (Odonata). Libellula Suppl 14:1–394Google Scholar
  9. Carere C, Gherardi F (2013) Animal personalities matter for biological invasions. Trends Ecol Evol 28:5–6. CrossRefPubMedGoogle Scholar
  10. Chen IC, Hill JK, Ohlemuller R et al (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026. CrossRefGoogle Scholar
  11. Chevin L, Lande R, Mace GM (2010) Adaptation, plasticity and extinction in a changing environment: towards a predictive theory. PLoS Biol 8:1–8. CrossRefGoogle Scholar
  12. Chuang A, Peterson CR (2016) Expanding population edges: theories, traits, and trade-offs. Glob Change Biol 22:494–512. CrossRefGoogle Scholar
  13. Clusella Trullas S, van Wyk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32:235–245. CrossRefGoogle Scholar
  14. Cordero A (1991) Fecundity of Ischnura graellsii (Rambur) in the laboratory (Zygoptera: Coenagrionidae). Odonatologica 20:37–44Google Scholar
  15. Cote J, Clobert J, Brodin T et al (2010) Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philos Trans R Soc B-Biol Sci 365:4065–4076. CrossRefGoogle Scholar
  16. Côte J, Boniface A, Blanchet S, Hendry AP, Gasparini J, Jacquin L (2018) Melanin-based coloration and host-parasite interactions under global change. Proc Roy Soc B. 285(1879):20180285CrossRefGoogle Scholar
  17. Cόrdoba-Aguilar A (2008) Dragonflies and damselflies: model organisms for ecological and evolutionary theory. Oxford Univ Press, OxfordCrossRefGoogle Scholar
  18. De Block M, Stoks R (2003) Adaptive sex-specific life history plasticity to temperature and photoperiod in a damselfly. J Evol Biol 16:986–995CrossRefGoogle Scholar
  19. De Block M, Stoks R (2007) Flight-related body morphology shapes mating success in a damselfly. Anim Behav 74:1093–1098. CrossRefGoogle Scholar
  20. De Block M, Slos S, Johansson F, Stoks R (2008) Integrating life history and physiology to understand latitudinal size variation in a damselfly. Ecography 31:115–123. CrossRefGoogle Scholar
  21. Deknijf G (1995) Crocothemis erythraea en Cercion lindenii, nu al in België en binnenkort ook in Nederland algemeen? Libellennieuwsbrief 4:7–12Google Scholar
  22. Dijkstra K-DB (2006) Field guide to the dragonflies of Britain and Europe. British Wildlife Publishing, DevonGoogle Scholar
  23. Dingemanse NJ, Wright J, Kazem AJN et al (2007) Behavioral syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Dommanget JL (1987) Etude faunistique et bibliographique des Odonates de France. Secrétariat Faune/Flore ParisGoogle Scholar
  25. Endler J (1995) Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol Evol 10:22–29. CrossRefPubMedGoogle Scholar
  26. Fedorka KM, Copeland EK, Winterhalter WE (2013) Seasonality influences cuticle melanization and immune defense in a cricket: support for a temperature-dependent immune investment hypothesis in insects. J Exp Biol 216:4005–4010. CrossRefPubMedGoogle Scholar
  27. Futahashi R (2016) Color vision and color formation un dragonflies. Curr Opin Insect Sci 17:32–39. CrossRefPubMedGoogle Scholar
  28. Garcia TS, Straus R, Sih A (2003) Temperature and ontogenetic effects on color change in the larval salamander species Ambystoma barbouri and Ambystoma texanum. Can J Zool-Rev Can Zool 81:710–715. CrossRefGoogle Scholar
  29. García-de-Lomas J, Vilà M (2015) Lists of harmful alien organisms: are the national regulations adapted to the global world? Biol Invasions 17:3081–3091. CrossRefGoogle Scholar
  30. Gaston KJ (2009) Geographic range limits: achieving synthesis. Proc R Soc B-Biol Sci 276:1395–1406. CrossRefGoogle Scholar
  31. González-Santoyo, Córdoba-Aguilar (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142:1–16. CrossRefGoogle Scholar
  32. Hardie DC, Hutchings JA (2010) Evolutionary ecology at the extremes of species’ ranges. Environ Rev 18:1–20. CrossRefGoogle Scholar
  33. Hill JK, Griffiths HM, Thomas CD (2011) Climate change and evolutionary adaptations at species’ range margins. Annu Rev Entomol 56:143–159. CrossRefPubMedGoogle Scholar
  34. Hodgetts RB, O’Keefe SL (2006) Dopa decarboxylase: a model gene-enzyme system for studying development, behavior, and systematics. Annu Rev Entomol 51:259–284. CrossRefPubMedGoogle Scholar
  35. Hughes CL, Dytham C, Hill JK (2007) Modelling and analyzing evolution of dispersal in populations at expanding range boundaries. Ecol Entomol 32:437–445CrossRefGoogle Scholar
  36. Kim S-Y, Velando A (2015) Phenotypic integration between antipredator behavior and camouflage pattern in juvenile sticklebacks. Evolution 69:830–838. CrossRefPubMedGoogle Scholar
  37. Lohr M (2003) Crocothemis erythraea auch in Niedersachsen (Odonata: Libellulidae). Libellula 22:35–39Google Scholar
  38. Mafli A, Wakamatsu K, Roulin A (2011) Melanin-based coloration predicts aggressiveness and boldness in captive eastern Hermann’s tortoises. Anim Behav 81:859–863. CrossRefGoogle Scholar
  39. Marden JH, Rowan B (2000) Growth, differential survival, and shifting sex ratio of free-living Libellula pulchella (Odonata: Libellulidae) dragonflies during adult maturation. Ann Entomol Soc Am 93:452–458. CrossRefGoogle Scholar
  40. Oberski DL (2014) lavaan.survey: an R package for complex survey analysis of structural equation models. J Stat Softw 57(1):1–27CrossRefGoogle Scholar
  41. Ott J (2007) The expansion of Crocothemis erythraea (Brullé, 1832) in Germany – an indicator of climatic changes. In: Tyagi BK (ed) Biology of dragonflies. Scientific Publishers, JodhpurGoogle Scholar
  42. Phillips BL, Brown GP, Shine R (2010) Life-history evolution in range-shifting populations. Ecology 91:1617–1627. CrossRefPubMedGoogle Scholar
  43. Pinkert, S, Brandl R, Zeuss D (2016) Colour lightness of dragonfly assemblages across North America and Europe. Ecography. CrossRefGoogle Scholar
  44. Pintor LM, Sih A, Bauer ML (2008) Differences in aggression, activity and boldness between native and introduced populations of an invasive crayfish. Oikos 117:1629–1636. CrossRefGoogle Scholar
  45. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  46. Raffard A, Cucherousset J, Prunier JG, Loot G, Santoul F, Blanchet S (2019) Variability of functional traits and their syndromes in a freshwater fish species (Phoxinus phoxinus): the role of adaptive and non-adaptive processes. Ecol Evolut 9:2833–2846CrossRefGoogle Scholar
  47. Roff DA, Fairbairn DJ (2012) The evolution of trade-offs under directional and correlational selection. Evolution 66:2461–2474. CrossRefPubMedGoogle Scholar
  48. Roff DA, Fairbairn DJ (2013) The costs of being dark: the genetic basis of melanism and its association with fitness-related traits in the sand cricket. J Evol Biol 26:1406–1416. CrossRefPubMedGoogle Scholar
  49. Schilder RJ, Marden JH (2004) A hierarchical analysis of the scaling of force and power production by dragonfly flight motors. J Exp Biol 207:767–776. CrossRefPubMedGoogle Scholar
  50. Stamps JA (2007) Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol Lett 5:355–363CrossRefGoogle Scholar
  51. Stoks R, Cόrdoba-Aguilar A (2012) Evolutionary ecology of Odonata: a complex life cycle perspective. Ann Rev Entomol 57:249–265CrossRefGoogle Scholar
  52. Therry L, Lefevre E, Bonte D, Stoks R (2014a) Increased activity and growth rate in the non-dispersive aquatic larval stage of a damselfly at an expanding range edge. Freshw Biol 59:1266–1277. CrossRefGoogle Scholar
  53. Therry L, Nilsson-Örtman V, Bonte D, Stoks R (2014b) Rapid evolution of larval life history, adult immune function and flight muscles in a poleward-moving damselfly. J Evol Biol 27:141–152. CrossRefPubMedGoogle Scholar
  54. Therry L, Gyulavari HA, Schillewaert S et al (2014c) Integrating large-scale geographic patterns in flight morphology, flight characteristics and sexual selection in a range-expanding damselfly. Ecography 37:1012–1021. CrossRefGoogle Scholar
  55. Therry L, Bonte D, Stoks R (2015) Higher investment in flight morphology does not trade off with fecundity estimates in a poleward range-expanding damselfly. Ecol Entomol 40:133–142CrossRefGoogle Scholar
  56. Therry L, Cote J, Cucherousset J et al (2019) Genetic and environmental contributions to the impact of a range-expanding predator on aquatic ecosystems. J Anim Ecol. CrossRefPubMedGoogle Scholar
  57. True JR (2003) Insect melanism: the molecules matter. Trends Ecol Evol 18:640–647. CrossRefGoogle Scholar
  58. Valiente AG, Juanes F, Nunez P, Garcia-Vazquez E (2010) Brown trout (Salmo trutta) invasiveness: plasticity in life-history is more important than genetic variability. Biol Invasions 12:451–462. CrossRefGoogle Scholar
  59. van Oers K, Mueller JC (2010) Evolutionary genomics of animal personality. Phil Trans R Soc B 365(1560):3991–4000CrossRefGoogle Scholar
  60. Verhoog MD, Breuker CJ, Brakefield PM (1998) The influence of genes for melanism on the activity of the flour moth, Ephestia kuehniella. Anim Behav 56:683–688. CrossRefPubMedGoogle Scholar
  61. Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality-rates mediated by foraging activity. Am Nat 142:242–272. CrossRefPubMedGoogle Scholar
  62. Zeuss D, Brandl R, Brändle M, Rahbek K, Brunzel S (2014) Global warming favours light-coloured insects in Europe. Nat Com 5:3874CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Centre Nationale Pour la Recherche Scientifique (CNRS)Université Paul Sabatier (UPS), Station d’Écologie Théorique et Expérimentale, UMR 5321MoulisFrance
  2. 2.Department of Aquaculture and Fish BiologyHólar University CollegeSauðárkrókurIceland
  3. 3.Institute of Life and Environmental Science, University of IcelandReykjavíkIceland
  4. 4.Department of Evolutionary EcologyJohannes Gutenberg-University MainzMainzGermany
  5. 5.Department of Ecology and Environmental ScienceUmeå UniversityUmeåSweden
  6. 6.CNRS, UPS, IRD, Laboratoire Évolution et Diversité BiologiqueUMR 5174ToulouseFrance

Personalised recommendations