Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-06-07T05:47:32.030Z Has data issue: false hasContentIssue false
  • English
  • Français

Shedding new light upon circadian emergence rhythmicity in the mountain pine beetle (Coleoptera: Curculionidae: Scolytinae)

Published online by Cambridge University Press:  15 April 2019

Debra L. Wertman  and
Katherine P. Bleiker
Debra L. Wertman*
Affiliation:
Department of Biology, University of Victoria, Cunningham Building, 3800 Finnerty Road, Victoria, British Columbia, V8P 5C2, Canada; and Pacific Forestry Centre, Natural Resources Canada – Canadian Forest Service, 506 W Burnside Road, Victoria, British Columbia, V8Z 1M5, Canada Pacific Forestry Centre, Natural Resources Canada – Canadian Forest Service, 506 W Burnside Road, Victoria, British Columbia, V8Z 1M5, Canada
Katherine P. Bleiker
Affiliation:
Pacific Forestry Centre, Natural Resources Canada – Canadian Forest Service, 506 W Burnside Road, Victoria, British Columbia, V8Z 1M5, Canada
*
2Corresponding author (e-mail: dwertman@uvic.ca)
Get access Rights & Permissions [Opens in a new window]

Abstract

The phenological behaviours of temperate insects can be highly controlled by photoperiod. Some foundational studies of the mountain pine beetle, Dendroctonus ponderosae (Hopkins) (Coleoptera: Curculionidae), documented a diurnal emergence rhythm that was asynchronous with maximum daily temperatures in the field and persisted under constant temperature and light conditions. In the 1970s, researchers hypothesised that this emergence rhythm was regulated by an endogenous circadian mechanism. Reflecting upon these historical data, we consider that a diurnal pattern of D. ponderosae emergence may result from photoperiodic entrainment of the circadian clock during the immature stages. Mechanistically, we suggest that the long-wavelength-sensitive opsin that we previously found to be expressed across D. ponderosae life stages could mediate, from beneath the bark, the input of light–dark cycle cues that are usually required for entrainment of the insect circadian clock.

Type
Forum
Information
The Canadian Entomologist , Volume 151 , Issue 3 , June 2019 , pp. 273 - 277
Copyright
© Entomological Society of Canada 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

1

Present address: Department of Forest and Conservation Sciences, Forest Sciences Centre, University of British Columbia, 3041 – 2424 Main Mall, Vancouver, British Columbia, V6T 1Z4, Canada.

Subject editor: Therese Poland

References

Beck, S.D. 1982. Thermoperiodic induction of larval diapause in the European corn borer, Ostrinia nubilalis. Journal of Insect Physiology, 28: 273–277. https://doi.org/10.1016/0022-1910(82)90087-7.CrossRefGoogle Scholar
Bentz, B.J., Logan, J.A., and Amman, G.D. 1991. Temperature-dependent development of the mountain pine beetle (Coleoptera: Scolytidae) and simulation of its phenology. The Canadian Entomologist, 123: 1083–1094. https://doi.org/10.4039/Ent1231083-5.CrossRefGoogle Scholar
Bentz, B.J., Vandygriff, J., Jensen, C., Coleman, T., Maloney, P., Smith, S., et al. 2013. Mountain pine beetle voltinism and life history characteristics across latitudinal and elevational gradients in the western United States. Forest Science, 60: 434–449. https://doi.org/10.5849/forsci.13-056.CrossRefGoogle Scholar
Billings, R.F. and Gara, R.I. 1975. Rhythmic emergence of Dendroctonus ponderosae (Coleoptera: Scolytidae) from two host species. Annals of the Entomological Society of America, 68: 1033–1036. https://doi.org/10.1093/aesa/68.6.1033.CrossRefGoogle Scholar
Bradshaw, W.E. and Holzapfel, C.M. 2007. Evolution of animal photoperiodism. Annual Review of Ecology, Evolution, and Systematics, 38: 1–25. https://doi.org/10.1146/annurev.ecolsys.37.091305.110115.CrossRefGoogle Scholar
Bradshaw, W.E. and Holzapfel, C.M. 2010. What season is it anyway? Circadian tracking vs. photoperiodic anticipation in insects. Journal of Biological Rhythms, 25: 155–165. https://doi.org/10.1177/0748730410365656.CrossRefGoogle ScholarPubMed
Buschbeck, E.K. and Friedrich, M. 2008. Evolution of insect eyes: tales of ancient heritage, deconstruction, reconstruction, remodeling, and recycling. Evolution: Education and Outreach, 1: 448–462. https://doi.org/10.1007/s12052-008-0086-z.Google Scholar
Doležal, P. and Sehnal, F. 2007. Effects of photoperiod and temperature on the development and diapause of the bark beetle Ips typographus. Journal of Applied Entomology, 131: 165–173. https://doi.org/10.1111/j.1439-0418.2006.01123.x.CrossRefGoogle Scholar
Emerson, K.J., Dake, S.J., Bradshaw, W.E., and Holzapfel, C.M. 2009. Evolution of photoperiodic time measurement is independent of the circadian clock in the pitcher-plant mosquito, Wyeomyia smithii. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology, 195: 385–391. https://doi.org/10.1007/s00359-009-0416-9.CrossRefGoogle ScholarPubMed
Felisberti, F., Ventura, D.F., and Hertel, H. 1997. Cerebral extraocular photoreceptors in beetles. Comparative Biochemistry and Physiology, 118A: 1353–1357. https://doi.org/10.1016/S0300-9629(97)00249-1.CrossRefGoogle Scholar
Friedrich, M. 2013. Biological clocks and visual systems in cave-adapted animals at the dawn of speleogenomics. Integrative and Comparative Biology, 53: 50–67. https://doi.org/10.1093/icb/ict058.CrossRefGoogle ScholarPubMed
Friedrich, M., Chen, R., Daines, B., Bao, R., Caravas, J., Rai, P.K., et al. 2011. Phototransduction and clock gene expression in the troglobiont beetle Ptomaphagus hirtus of Mammoth Cave. Journal of Experimental Biology, 214: 3532–3541. https://doi.org/10.1242/jeb.060368.CrossRefGoogle ScholarPubMed
Gray, B., Billings, R.F., Gara, R.I., and Johnsey, R.L. 1972. On the emergence and initial flight behaviour of the mountain pine beetle, Dendroctonus ponderosae, in eastern Washington. Zeitschrift Fur Angewandte Entomologie, 71: 250–259. https://doi.org/10.1111/j.1439-0418.1972.tb01745.x.CrossRefGoogle Scholar
Helfrich-Förster, C., Winter, C., Hofbauer, A., Hall, J.C., and Stanewsky, R. 2001. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron, 30: 249–261. https://doi.org/10.1016/S0896-6273(01)00277-X.CrossRefGoogle ScholarPubMed
Jackowska, M., Bao, R., Liu, Z., McDonald, E.C., Cook, T.A., and Friedrich, M. 2007. Genomic and gene regulatory signatures of cryptozoic adaptation: loss of blue sensitive photoreceptors through expansion of long-wavelength-opsin expression in the red flour beetle Tribolium castaneum. Frontiers in Zoology, 4: 1–11. https://doi.org/10.1186/1742-9994-4-24.CrossRefGoogle ScholarPubMed
Jordal, B.H. 2014. Scolytinae Latreille, 1806. In Arthropoda: Insecta: Coleoptera; volume 3: morphology and systematics (Phytophaga). Edited by Leschen, R.A.B. and Beutel, R.G.. De Gruyter, Berlin, Germany. Pp. 633–642.Google Scholar
Keeling, C.I., Yuen, M.M.S., Liao, N.Y., Roderick Docking, T., Chan, S.K., Taylor, G.A., et al. 2013. Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biology, 14: 1–19. https://doi.org/10.1186/gb-2013-14-3-r27.CrossRefGoogle ScholarPubMed
Lampel, J., Briscoe, A.D., and Wasserthal, L.T. 2005. Expression of UV-, blue-, long-wavelength-sensitive opsins and melatonin in extraretinal photoreceptors of the optic lobes of hawkmoths. Cell and Tissue Research, 321: 443–458. https://doi.org/10.1007/s00441-004-1069-1.CrossRefGoogle Scholar
National Centre for Biotechnology Information Resource Coordinators. 2017. Database resources of the National Center for Biotechnology Information. Nucleic Acids Research, 45: D12–D17. https://doi.org/10.1093/nar/gkw1071.CrossRefGoogle Scholar
Paiva, M.R. and Vité, J.P. 1982. Breaking of the diapause of Trypodendron lineatum (Oliv.) (Col., Scolytidae) by cold shock treatments. Zeitschrift für Angewandte Entomologie, 93: 347–355. https://doi.org/10.1111/j.1439-0418.1982.tb03607.x.CrossRefGoogle Scholar
Reid, R.W. 1962. Biology of the mountain pine beetle, Dendroctonus monticolae Hopkins, in the East Kootenay region of British Columbia. I. Life cycle, brood development and flight periods. The Canadian Entomologist, 94: 531–538. https://doi.org/10.4039/Ent94531-5.CrossRefGoogle Scholar
Safranyik, L. 1978. Effects of climate and weather on mountain pine beetle populations. In Proceedings of symposium on theory and practice of mountain pine beetle management in lodgepole pine forests, Washington State University, Pullman, Washington, 25–27 April 1978. Edited by Berryman, A.A., Amman, G.D., and Stark, R.W.. College of Forestry, Wildlife and Range Sciences, University of Idaho, Moscow, Idaho, United States of America. Pp. 77–84.Google Scholar
Safranyik, L. and Carroll, A. 2006. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests. In The mountain pine beetle: a synthesis of biology, management, and impacts on lodgepole pine. Edited by Safranyik, L. and Wilson, W.R.. Natural Resources Canada, Canadian Forest Service, Pacific Forestry Centre, Victoria, British Columbia, Canada. Pp. 3–66.Google Scholar
Safranyik, L., Carroll, A.L., Régnière, J., Langor, D.W., Riel, W.G., Shore, T.L., et al. 2010. Potential for range expansion of mountain pine beetle into the boreal forest of North America. The Canadian Entomologist, 142: 415–442. https://doi.org/10.4039/n08-CPA01.CrossRefGoogle Scholar
Saunders, D.S. 1973. Thermoperiodic control of diapause in an insect: theory of internal coincidence. American Association for the Advancement of Science, 181: 358–360. https://doi.org/10.1126/science.181.4097.358.CrossRefGoogle Scholar
Saunders, D.S. 2012. Insect photoperiodism: seeing the light. Physiological Entomology, 37: 207–218. https://doi.org/10.1111/j.1365-3032.2012.00837.x.CrossRefGoogle Scholar
Saunders, D.S. 2014. Insect photoperiodism: effects of temperature on the induction of insect diapause and diverse roles for the circadian system in the photoperiodic response. Entomological Science, 17: 25–40. https://doi.org/10.1111/ens.12059.CrossRefGoogle Scholar
Shepherd, R.F. 1966. Factors influencing the orientation and rates of activity of Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae). The Canadian Entomologist, 98: 507–518. https://doi.org/10.4039/Ent98507-5.CrossRefGoogle Scholar
Shimizu, I., Yamakawa, Y., Shimazaki, Y., and Iwasa, T. 2001. Molecular cloning of Bombyx cerebral opsin (boceropsin) and cellular localization of its expression in the silkworm brain. Biochemical and Biophysical Research Communications, 287: 27–34. https://doi.org/10.1006/bbrc.2001.5540.CrossRefGoogle ScholarPubMed
Shintani, Y. 2011. Quantitative short-day photoperiodic response in larval development and its adaptive significance in an adult-overwintering cerambycid beetle, Phytoecia rufiventris. Journal of Insect Physiology, 57: 1053–1059. https://doi.org/10.1016/j.jinsphys.2011.05.005.CrossRefGoogle Scholar
Shintani, Y., Ishikawa, Y., and Tatsuki, S. 1996. Larval diapause in the yellow-spotted longicorn beetle, Psacothea hilaris (Pascoe) (Coleoptera: Cerambycidae). Applied Entomology and Zoology, 31: 489–494. https://doi.org/10.1303/aez.31.489.CrossRefGoogle Scholar
Spaethe, J. and Briscoe, A.D. 2005. Molecular characterization and expression of the UV opsin in bumblebees: three ommatidial subtypes in the retina and a new photoreceptor organ in the lamina. Journal of Experimental Biology, 208: 2347–2361. https://doi.org/10.1242/jeb.01634.CrossRefGoogle Scholar
Tierney, S.M., Friedrich, M., Humphreys, W.F., Jones, T.M., Warrant, E.J., and Wcislo, W.T. 2017. Consequences of evolutionary transitions in changing photic environments. Austral Entomology, 56: 23–46. https://doi.org/10.1111/aen.12264.CrossRefGoogle Scholar
Velarde, R.A., Sauer, C.D., Walden, K.K.O., Fahrbach, S.E., and Robertson, H.M. 2005. Pteropsin: a vertebrate-like non-visual opsin expressed in the honey bee brain. Insect Biochemistry and Molecular Biology, 35: 1367–1377. https://doi.org/10.1016/j.ibmb.2005.09.001.CrossRefGoogle ScholarPubMed
Watson, J.A. 1970. Rhythmic emergence patterns of the mountain pine beetle Dendroctonus ponderosae (Coleoptera: Scolytidae). The Canadian Entomologist, 102: 1054–1056. https://doi.org/10.4039/Ent1021054-8.CrossRefGoogle Scholar
Wertman, D.L., Bleiker, K.P., and Perlman, S.J. 2018. The light at the end of the tunnel: photosensitivity in larvae of the mountain pine beetle (Coleoptera: Curculionidae: Scolytinae). The Canadian Entomologist, 150: 622–631. https://doi.org/10.4039/tce.2018.38.CrossRefGoogle Scholar
Yuan, Q., Metterville, D., Briscoe, A.D., and Reppert, S.M. 2007. Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. Molecular Biology and Evolution, 24: 948–955. https://doi.org/10.1093/molbev/msm011.CrossRefGoogle ScholarPubMed