Autumn shifts in cold tolerance metabolites in overwintering adult mountain pine beetles

Autoři: Kirsten M. Thompson aff001;  Dezene P. W. Huber aff001;  Brent W. Murray aff001
Působiště autorů: Natural Resources and Environmental Studies, University of Northern British Columbia, Prince George, British Columbia, Canada aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


The mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae) is a major forest pest of pines in western North America. Beetles typically undergo a one-year life cycle with larval cold hardening in preparation for overwintering. Two-year life cycle beetles have been observed but not closely studied. This study tracks cold-hardening and preparation for overwintering by adult mountain pine beetles in their natal galleries. Adults were collected in situ between September and December 2016 for a total of nine time points during 91 days. Concentrations of 41 metabolites in these pooled samples were assessed using quantitative nuclear magnetic resonance (NMR). Levels of glycerol and proline increased significantly with lowering temperature during the autumn. Newly eclosed mountain pine beetles appear to prepare for winter by generating the same cold-tolerance compounds found in other insect larvae including mountain pine beetle, but high on-site mortality suggested that two-year life cycle adults have a less efficacious acclimation process. This is the first documentation of cold acclimation metabolite production in overwintering new adult beetles and is evidence of physiological plasticity that would allow evolution by natural selection of alternate life cycles (shortened or lengthened) under a changing climate or during expansion into new geoclimatic areas.

Klíčová slova:

Beetles – Life cycles – Larvae – Proline – Glycerol – Metabolites – Pines – Trehalose


1. Bracewell RR, Bentz BJ, Sullivan BT, Good JM. Rapid neo-sex chromosome evolution and incipient speciation in a major forest pest. Nat Commun. 2017;8: 1593. doi: 10.1038/s41467-017-01761-4 29150608

2. Hrinkevich K, Lewis KJ. Northern range limit mountain pine beetle outbreak dynamics in mixed sub-boreal pine forests of British Columbia. Ecosphere. 2011;2: 1–16. doi: 10.1890/ES11-00150.1

3. Cullingham CI, Cooke JEK, Dang S, Davis CS, Cooke BJ, Coltman DW. Mountain pine beetle host-range expansion threatens the boreal forest. Mol Ecol. 2011;20: 2157–2171. doi: 10.1111/j.1365-294X.2011.05086.x 21457381

4. Janes JK, Li Y, Keeling CI, Yuen MMS, Boone CK, Cooke JEK, et al. How the Mountain Pine Beetle (Dendroctonus ponderosae) Breached the Canadian Rocky Mountains. Mol Biol Evol. 2014;31: 1803–1815. doi: 10.1093/molbev/msu135 24803641

5. Safranyik L, Linton DA. Mortality of mountain pine beetle larvae, Dendroctonus ponderosae (Coleoptera: Scolytidae) in logs of lodgepole pine (Pinus contorta var. latifolia) at constant low temperatures. J Entomol Soc Br Columbia. 1998;95: 81–88. Available:

6. Safranyik L, Carroll AL. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests. The Mountain Pine Beetle: A Synthesis of Biology, Management, and Impacts on Lodgepole Pine. Canadian Forest Service; 2006. pp. 3–66.

7. Carroll AL, Taylor SW, Regniere J, Safranyik L. Effect of climate change on range expansion by the mountain pine beetle in British Columbia [Internet]. The Bark Beetles, Fuels, and Fire Bibliography. Paper 195. 2003. pp. 223–232. Available:

8. Goodsman DW, Grosklos G, Aukema BH, Whitehouse C, Bleiker KP, McDowell NG, et al. The effect of warmer winters on the demography of an outbreak insect is hidden by intraspecific competition. Glob Chang Biol. 2018;24: 3620–3628. doi: 10.1111/gcb.14284 29808947

9. Bentz BJ, Régnière J, Fettig CJ, Hansen M, Hayes JL, Hicke JA, et al. Climate change and bark beetles of the western United States and Canada: Direct and indirect effects. Bioscience. 2010;60: 602–613. doi: 10.1525/bio.2010.60.8.6

10. Six DL, Bracewell RR. Dendroctonus. In: Vega FE, Hofstetter RW, editors. Bark Beetles: Biology and Ecology of Native and Invasive Species. 1st ed. London: Academic Press; 2015. pp. 305–350.

11. Bentz BJ, Powell JA. Mountain pine beetle seasonal timing and constraints to bivoltinism (A comment on Mitton and Ferrenberg,"Mountain pine beetle develops an unprecedented summer generation in response to climate warming”). Am Nat. 2014;184: 787–796. doi: 10.1086/678405 25438178

12. Bentz BJ, Mullins DE. Ecology of mountain pine beetle (Coleoptera: Scolytidae) cold hardening in the Intermountain West. Physiol Chem Ecol. 1991;28: 577–587. doi: 10.1093/ee/28.4.577

13. Régnière J, Bentz B. Modeling cold tolerance in the mountain pine beetle, Dendroctonus ponderosae. J Insect Physiol. 2007;53: 559–572. doi: 10.1016/j.jinsphys.2007.02.007 17412358

14. Bleiker KP, Smith GD, Humble LM. Cold tolerance of mountain pine beetle (Coleoptera: Curculionidae) eggs from the historic and expanded ranges. Environ Entomol. 2017;46: 1165–1170. doi: 10.1093/ee/nvx127 28961978

15. Fraser JD, Bonnett TR, Keeling CI, Huber DPW. Seasonal shifts in accumulation of glycerol biosynthetic gene transcripts in mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Curculionidae), larvae. PeerJ. 2017;5: e3284. doi: 10.7717/peerj.3284 28626604

16. Robert JA, Bonnett T, Pitt C, Spooner LJ, Fraser J, Yuen MMS, et al. Gene expression analysis of overwintering mountain pine beetle larvae suggests multiple systems involved in overwintering stress, cold hardiness, and preparation for spring development. PeerJ. 2016;4: e2109. doi: 10.7717/peerj.2109 27441109

17. Logan JA, Bolstad P V, Bentz BJ, Perkins DL. Assessing the effects of changing climate on mountain pine beetle dynamics. Proceedings: Interior West Global Change Workshop, 25–27 April 1995, Fort Collins, CO. 1995. pp. 92–105. Available: etal_Assessing the Effects of Changing Climate.pdf

18. Keeling CI, Yuen MMS, Liao NY, Roderick Docking T, Chan SK, Taylor GA, et al. Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol. 2013;14: R27. doi: 10.1186/gb-2013-14-3-r27 23537049

19. Wertman DL, Bleiker KP, Perlman SJ. The light at the end of the tunnel: Photosensitivity in larvae of the mountain pine beetle (Coleoptera: Curculionidae: Scolytinae). Can Entomol. 2018;150: 622–631. doi: 10.4039/tce.2018.38

20. Amman GD. Population changes of the mountain pine beetle in relation to elevation. Environ Entomol. 1973;2: 541–548. doi: 10.1093/ee/2.4.541

21. Storey JM, Storey KB. Regulation of cryoprotectant metabolism in the overwintering gall fly larva, Eurosta solidaginis: Temperature control of glycerol and sorbitol levels. J Comp Physiol. 1983;149: 495–502. doi: 10.1007/BF00690008

22. Bonnett TR, Robert JA, Pitt C, Fraser JD, Keeling CI, Bohlmann J, et al. Global and comparative proteomic profiling of overwintering and developing mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae), larvae. Insect Biochem Mol Biol. 2012;42: 890–901. doi: 10.1016/j.ibmb.2012.08.003 22982448

23. DeLeon D, Bedard WD, Terrell TT. Recent discoveries concerning the biology of the mountain pine beetle and their effect on control in western white pine stands. J For. 1934;32: 430–436. doi: 10.1093/jof/32.4.430

24. Chong J, Xia J. MetaboAnalystR: an R package for flexible and reproducible analysis of metabolomics data. Bioinformatics. 2018;27: 4313–4314.

25. Miller LK, Werner RA. Cold-hardiness of adult and larval spruce beetles Dendroctonus rufipennis (Kirby) in interior Alaska. Can J Zool. 1987;65: 2927–2930. doi: 10.1139/z87-444

26. Wang J, Zhang RR, Gao GQ, Ma MY, Chen H. Cold tolerance and silencing of three cold-tolerance genes of overwintering Chinese white pine larvae. Sci Rep. 2016;6: 34698. doi: 10.1038/srep34698 27703270

27. Leather SR, Walters KFA, Bale JS. The ecology of insect overwintering. Cambridge: Cambridge University Press; 1995.

28. Storey K, Storey J. Insect cold hardiness: metabolic, gene, and protein adaptation. Can J Zool. 2012;90: 456–475. doi: 10.1139/z2012-014

29. Thompson SN. Trehalose-The insect ‘blood’ sugar. Adv In Insect Phys. 2003;31: 205–285. doi: 10.1016/S0065-2806(03)31004-5

30. Koštál V, Doležal P, Rozsypal J, Moravcová M, Zahradníčková H, Šimek P. Physiological and biochemical analysis of overwintering and cold tolerance in two Central European populations of the spruce bark beetle, Ips typographus. J Insect Physiol. 2011;57: 1136–1146. doi: 10.1016/j.jinsphys.2011.03.011 21420974

31. Feng Y, Xu L, Li W, Xu Z, Cao M, Wang J, et al. Seasonal changes in supercooling capacity and major cryoprotectants of overwintering Asian longhorned beetle (Anoplophora glabripennis) larvae. Agric For Entomol. 2016;18: 302–312. doi: 10.1111/afe.12162

32. Pemberton TA, Still BR, Christensen EM, Singh H, Srivastava D, Tanner JJ. Proline: Mother Nature’s cryoprotectant applied to protein crystallography. Acta Crystallogr Sect D. 2012;68: 1010–1018. doi: 10.1107/S0907444912019580 22868767

33. Carrasco MA, Buechler SA, Arnold RJ, Sformo T, Barnes BM, Duman JG. Investigating the deep supercooling ability of an Alaskan beetle, Cucujus clavipes puniceus, via high throughput proteomics. J Proteomics. 2012;75: 1220–1234. doi: 10.1016/j.jprot.2011.10.034 22094879

34. Teulier L, Weber JM, Crevier J, Darveau CA. Proline as a fuel for insect flight: Enhancing carbohydrate oxidation in hymenopterans. Proc R Soc B. 2016;283. doi: 10.1098/rspb.2016.0333 27412285

35. Gäde G, Auerswald L. Beetles’ choice-Proline for energy output: control by AKHs. Comp Biochem Physiol Part B. 2002;132: 117–129. doi: 10.1016/S1096-4959(01)00541-3

36. Pitt C, Robert JA, Bonnett TR, Keeling CI, Bohlmann J, Huber DPW. Proteomics indicators of the rapidly shifting physiology from whole mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae), adults during early host colonization. PLoS One. 2014;9: e110673. doi: 10.1371/journal.pone.0110673 25360753

37. Elnitsky MA, Hayward SAL, Rinehart JP, Denlinger DL, Lee RE. Cryoprotective dehydration and the resistance to inoculative freezing in the Antarctic midge, Belgica antarctica. J Exp Biol. 2008;211: 524–530. doi: 10.1242/jeb.011874 18245628

38. Bentz BJ, Duncan JP, Powell JA. Elevational shifts in thermal suitability for mountain pine beetle population growth in a changing climate. Forestry. 2016;89: 271–283. doi: 10.1093/forestry/cpv054

Článok vyšiel v časopise


2020 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.


Nemáte účet?  Registrujte sa