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Northward range expansion requires synchronization of both overwintering behaviour and physiology with photoperiod in the invasive Colorado potato beetle (Leptinotarsa decemlineata)

  • Physiological ecology - Original research
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Abstract

Photoperiodic phenological adaptations are prevalent in many organisms living in seasonal environments. As both photoperiod and growth season length change with latitude, species undergoing latitudinal range expansion often need to synchronize their life cycle with a changing photoperiod and growth season length. Since adaptive synchronization often involves a large number of time-consuming genetic changes, behavioural plasticity might be a faster way to adjust to novel conditions. We compared behavioural and physiological traits in overwintering (diapause) preparation in three latitudinally different European Colorado potato beetle (Leptinotarsa decemlineata) populations reared under two photoperiods. Our aim was to study whether behavioural plasticity could play a role in rapid range expansion into seasonal environments. Our results show that while burrowing into the soil occurred in the southernmost studied population also under a non-diapause-inducing long photoperiod, the storage lipid content of these beetles was very low compared to the northern populations. However, similar behavioural plasticity was not found in the northern populations. Furthermore, the strongest suppression of energy metabolism was seen in pre-diapause beetles from the northernmost population. These results could indicate accelerated diapause preparation and possibly energetic adjustments due to temporal constraints imposed by a shorter, northern, growth season. Our results indicate that behavioural plasticity in burrowing may have facilitated initial range expansion of L. decemlineata in Europe. However, long-term persistence at high latitudes has required synchronization of burrowing behaviour with physiological traits. The results underline that eco-physiological life-history traits of insects, such as diapause, should be included in studies on range expansion.

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References

  • Alyokhin AV (2009) Colorado potato beetle management on potatoes: current challenges and future prospects. Fruit Veg Cereal Sci Biotech 3:10–19

    Google Scholar 

  • Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bean DW, Dalin P, Dudley TL (2012) Evolution of critical day length for diapause induction enables range expansion of Diorhabda carinulata, a biological control agent against tamarisk (Tamarix spp.). Evol App 5:511–523

    Article  Google Scholar 

  • Beck SD, Hanec W (1960) Diapause in the European corn borer, Pyrausta nubialis (Hübn.). J Insect Physiol 4:304–318

    Article  Google Scholar 

  • Beekman M, van Stratum P, Lingeman R (1998) Diapause survival and post-diapause performance in Bumblebee queens (Bombus terrestris). Entomol Exp Appl 89:207–214

    Article  Google Scholar 

  • Block W, Young SR (1978) Metabolic adaptations of Antarctic terrestrial micro arthropods. Comp Biochem Physiol 61A:363–368

    Article  CAS  Google Scholar 

  • Boiteau G, Coleman W (1996) Cold tolerance in the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Can Entomol 128:1087–1099

    Article  Google Scholar 

  • Boman S, Grapputo A, Lindström L, Lyytinen A, Mappes J (2008) Quantitative genetic approach for assessing invasiveness: geographic and genetic variation in life-history traits. Biol Invasions 10:1135–1145

  • Bradshaw WE, Holzapfel CM (2001) Genetic shift in photoperiodic response correlated with global warming. Proc Nat Acad Sci USA 98:14509–14511

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bradshaw WE, Holzapfel CM (2007) Evolution of animal photoperiodism. Ann Rev Ecol Evol Syst 3:1–25

    Article  Google Scholar 

  • Casagrande RA (1987) The Colorado potato beetle: 125 years of mismanagement. Bull Entomol Soc Am 33:142–150

    Google Scholar 

  • Chown SL, Gaston K (1999) Exploring links between physiology and ecology at macro-scales: the role of respiratory metabolism in insects. Biol Rev 74:87–120

    Article  Google Scholar 

  • Chown SL, Nicolson SW (2004) Insect physiological ecology—mechanisms and patterns. Oxford University Press, New York

    Google Scholar 

  • Clarke A (1993) Seasonal acclimatization and latitudinal compensation in metabolism: do they exist? Funct Ecol 7:139–149

    Article  Google Scholar 

  • Costanzo JP, Humphreys TL, Lee RE Jr, Moore JB, Lee MR, Wyman JA (1998) Long-term reduction of cold hardiness following ingestion of ice-nucleating bacteria in the Colorado potato beetle, Leptinotarsa decemlineata. J Insect Physiol 44:1173–1180

  • Danilevski AS (1965) Photoperiodism and seasonal development of insects. Oliver and Boyd, London

    Google Scholar 

  • Danks HV (1987) Insect dormancy: an ecological perspective. Biological Survey of Canada (Terrestrial Arthropods), Ottawa. Biological Survey of Canada Monograph Series No. 1

  • de Kort CAD (1990) Thirty-five years of diapause research with the Colorado potato beetle. Entomol Exp Appl 56:1–13

    Article  Google Scholar 

  • Duckworth RA (2009) The role of behavior in evolution: a search for mechanism. Evol Ecol 23:513–531

    Article  Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Melthuen & Co, London

    Book  Google Scholar 

  • EPPO (2006) Distribution maps of quarantine pests for Europe, Leptinotarsa decemlineata. ADAS, Nottingham, UK. Available at: http://pqr.eppo.org/datas/LPTNDE/LPTNDE.pdf

  • Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Gabel F, Pusch MT, Breyer P, Burmester V, Walz N, Garcia X (2011) Differential effect of wave stress on the physiology and behaviour of native versus non native benthic invertebrates. Biol Invasions 13:1843–1853

    Article  Google Scholar 

  • Gaston K (2003) The structure and dynamics of geographic ranges. Oxford series in ecology and evolution. Oxford University Press, New York

    Google Scholar 

  • Gomi T (2007) Seasonal adaptations of the fall webworm Hypantria cunea (Drury) (Lepidoptera:Arctiidae) following its invasion of Japan. Ecol Res 22:855–861

    Article  Google Scholar 

  • Grapputo A, Boman S, Lindström L, Lyytinen A, Mappes J (2005) The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 14:4207–4219

    Article  CAS  PubMed  Google Scholar 

  • Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 74:1–40

    Article  CAS  PubMed  Google Scholar 

  • Hack MA (1997) The effects of mass and age on standard metabolic rate in house crickets. Physiol Entomol 22:325–331

    Article  Google Scholar 

  • Hahn DA, Denlinger DL (2007) Meeting the energetic demands of insect diapause: nutrient storage and utilization. J Insect Physiol 53:760–773

    Article  CAS  PubMed  Google Scholar 

  • Hanshew BA, Garcia TS (2012) Invasion of the shelter snatchers: behavioural plasticity in invasive red swamp crayfish, Procambarus clarkii. Freshwater Biol 57:2285–2296

    Article  Google Scholar 

  • Hodkova M, Hodek I (2004) Photoperiod, diapause and cold-hardiness. Eur J Entomol 101:445–458

    Article  Google Scholar 

  • Hsiao TH (1985) Eco-physiological and genetic aspects of geographic variations of the Colorado potato beetle. Res Bull Mass Agric Exp Stn 704:63–77

    Google Scholar 

  • Izzo VM, Hawthorne DJ, Chen YH (2013) Geographic variation in winter hardiness of a common agricultural pest, Leptinotarsa decemlineata, the Colorado potato beetle. Evol Ecol, (accepted) Online Version. doi:10.1007/s10682-013-9681-8

  • Johnson CG (1967) International dispersal of insects and insect-borne viruses. Eur J Plant Pathol 73:21–43

    Google Scholar 

  • Jönsson AM, Pulatov B, Linderson M-J, Hall K (2013) Modelling as a tool for analysing the temperature-dependent future of the Colorado potato beetle in Europe. Glob Change Biol 19:1043–1055

    Article  Google Scholar 

  • Kenneth P, Case TJ (1996) An experimental demonstration of exploitation competition in an ongoing invasion. Ecology 77:118–132

    Article  Google Scholar 

  • Kostal V (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52:113–127

    Article  CAS  PubMed  Google Scholar 

  • Kuang X, Xu J, Xia Q, He H, Xue F (2011) Inheritance of the photoperiodic response controlling imaginal summer diapause in the Cabbage beetle, Colaphellus bowringii. J Insect Physiol 57:614–619

    Article  CAS  PubMed  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Lefevere KS, de Kort CAD (1989) Adult diapause in the Colorado potato beetle, Leptinotarsa decemlineata: effects of external factors on maintenance, termination and post-diapause development. Physiol Entomol 14:299–308

    Article  Google Scholar 

  • Lehmann P, Lyytinen A, Sinisalo T, Lindström L (2012) Population dependent effects of photoperiod on diapause related physiological traits in an invasive beetle (Leptinotarsa decemlineata). J Insect Physiol 58:1146–1158

    Article  CAS  PubMed  Google Scholar 

  • Lehmann P, Piiroinen S, Kankare M, Lyytinen A, Paljakka M, Lindström L (2014) Photoperiodic effects on diapause-associated gene expression trajectories in European Leptinotarsa decemlineata populations. Insect Mol Biol (in press)

  • Lighton JRB (2008) Measuring metabolic rates. Oxford University Press, New York

  • Lyytinen A, Mappes J, Lindström L (2012) Variation in Hsp70 levels after cold shock: signs of evolutionary responses to thermal selection among Leptinotarsa decemlineata populations. PLoS One 7:e31446

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mahdjoub T, Menu F (2008) Prolonged diapause: a trait increasing invasion speed? J Theor Biol 251:317–330

    Article  PubMed  Google Scholar 

  • May ML (1989) Oxygen consumption by adult Colorado potato beetles, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). J Insect Physiol 35:797–804

    Article  Google Scholar 

  • Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14

    Article  PubMed Central  PubMed  Google Scholar 

  • Nelson RJ, Denlinger DL, Somers DE (eds) (2010) Photoperiodism, the biological calendar. Oxford University Press, Oxford

    Google Scholar 

  • Phillips BL, Suarez AV (2012) The role of behavioural variation in the invasion of new areas. In: Candolin U, Wong BM (eds) Behavioural responses to a changing world: mechanisms and consequences. Oxford University Press, Oxford

    Google Scholar 

  • Pigliucci M, Murren CJ (2003) Genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution 57:1455–1464

    Article  PubMed  Google Scholar 

  • Piiroinen S, Lindström L, Lyytinen A (2010) Resting metabolic rate can vary with age independently from body mass changes in the Colorado potato beetle, Leptinotarsa decemlineata. J Insect Physiol 56:277–282

    Article  CAS  PubMed  Google Scholar 

  • Piiroinen S, Ketola T, Lyytinen A, Lindström L (2011) Energy use, diapause behaviour and northern range expansion potential in the invasive Colorado potato beetle. Funct Ecol 25:527–536

    Article  Google Scholar 

  • Piiroinen S, Lindström L, Lyytinen A, Mappes J, Chen YH, Izzo V, Grapputo A (2013) Pre-invasion history and demography shape the genetic variation in the insecticide resistance-related acetylcholinesterase 2 gene in the invasive Colorado potato beetle. BMC Evol Biol 13:13

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Randall D, Burggren W, French K (eds) (2002) Animal physiology. Freeman and Company, New York

    Google Scholar 

  • Rasa OAE (1999) Division of labour and extended parenting in a desert tenebrioid beetle. Ethology 105:37–56

    Article  Google Scholar 

  • Rankin MA, Burchsted JCA (1992) The cost of migration in insects. Annu Rev Entomol 37:533–559

    Article  Google Scholar 

  • Roubik DW, Michener CD (1980) The seasonal cycle and nests of Epicharis zonata, a bee whose cells are below the wet-season water table (Hymenoptera, Anthophoridae). Biotrop 12:56–60

    Article  Google Scholar 

  • Roberts SB, Rosenberg I (2006) Nutrition and aging: changes in the regulation of energy metabolism with aging. Physiol Rev 86:651–667

    Article  CAS  PubMed  Google Scholar 

  • Sagata K, Lester PJ (2009) Behavioural plasticity associated with propagule size, resources, and the invasion success of the Argentine ant Linepithema humile. J App Ecol 46:19–27

    Article  Google Scholar 

  • Saikkonen K, Taulavuori K, Hyvönen T, Gundel PE, Hamilton CE, Vänninen I, Nissinen A, Helander M (2012) Climate change-driven species’ range shifts filtered by photoperiodism. Nat Clim Change 2:239–242

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Mologsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thomspon JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Sexton JP, McKay JK, Sala A (2002) Plasticity and genetic diversity may allow saltcedar to invade cold climate in North America. Ecol Appl 12:1652–1660

    Article  Google Scholar 

  • Sinclair BJ, Bretman A, Tregenza T, Tomkins JL, Hosken DJ (2011) Metabolic rate does not decrease with starvation in Gryllus bimaculatus when changing fuel use is taken into accound. Physiol Entomol 36:84–89

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (2003) Biometry, the principles and practice of statistics in biological research. W.H.Freeman and Company, New York

    Google Scholar 

  • Solbreck C, Windefalk O (2012) Very long diapause and extreme resistance to population disturbance in a galling insect. Ecol Entomol 37:51–55

    Article  Google Scholar 

  • Sunday JM, Bates AE, Kearney MR, Colwell RK, Dulvy NK, Longino JT, Huey RB (2014) Thermal–safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc Nat Acad Sci USA 111:5610–5615

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, New York

    Google Scholar 

  • Tauber MJ, Tauber CA, Obrycki JJ, Gollands B, Wright RJ (1988) Voltinism and the induction of aestival diapause in the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). University of Nebraska, Faculty Publications: Department of Entomology, Paper 109

  • Urbanski J, Mogi M, O’Donnell D, DeCotiis M, Toma T, Armbruster P (2012) Rapid adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. Am Nat 179:490–500

    Article  PubMed  Google Scholar 

  • Valosaari KR, Aikio S, Kaitala V (2008) Spatial simulation model to predict the Colorado potato beetle invasion under different management strategies. Annls Zool Fenn 45:1–14

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

    Google Scholar 

  • Williams CM, Thomas RH, MacMillan HA, Marshall KE, Sinclair BJ (2011) Triacylglyceride measurement in small quantities of homogenised insect tissue: comparisons and caveats. J Insect Physiol 57:1602–1613

    Article  CAS  PubMed  Google Scholar 

  • Williams JB, Lee RE Jr (2008) Differences in cold tolerance, desiccation resistance, and cryoprotectant production between three populations of Eurosta solidaginis collected from different latitudes. J Comp Physiol B 178:365–375

    Article  PubMed  Google Scholar 

  • Wright TF, Eberhard JR, Hobson EA, Avery ML, Russello MA (2010) Behavioral flexibility and species invasions: the adaptive flexibility hypothesis. Ethol Ecol Evol 22:393–404

    Article  Google Scholar 

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Acknowledgments

We thank Alessandro Grapputo and Magdalena Szuplewska for providing beetles, Aigi Margus for sample analysis and Tanja Heikkilä for help with the rearing of the beetles. Karl Gotthard, Thomas Flatt, Daniel Hahn and anonymous reviewers are thanked for making valuable comments to improve this manuscript. This work was financed by The Academy of Finland: project numbers 250248, 263742 and 252411 (Finnish Centre of Excellence in Biological Interactions Research). L. decemlineata is a quarantine species in Finland, and therefore this experiment was carried out under permission (Evira 3861/541/2007).

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  1. Department of Biological and Environmental Science, Centre of Excellence in Biological Interactions Research, University of Jyväskylä, P.O. Box 35, 40014, Jyväskylä, Finland

    Philipp Lehmann, Anne Lyytinen, Saija Piiroinen & Leena Lindström

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  1. Philipp Lehmann
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Correspondence to Philipp Lehmann.

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Communicated by Sylvain Pincebourde.

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Lehmann, P., Lyytinen, A., Piiroinen, S. et al. Northward range expansion requires synchronization of both overwintering behaviour and physiology with photoperiod in the invasive Colorado potato beetle (Leptinotarsa decemlineata). Oecologia 176, 57–68 (2014). https://doi.org/10.1007/s00442-014-3009-4

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