Hostname: page-component-848d4c4894-p2v8j Total loading time: 0.001 Render date: 2024-05-17T14:07:09.800Z Has data issue: false hasContentIssue false
  • English
  • Français

Swede midge (Diptera: Cecidomyiidae) diapause initiation under stable conditions: not a family affair

Published online by Cambridge University Press:  07 June 2019

Lauren E. Des Marteaux Open the ORCID record for Lauren E. Des Marteaux [Opens in a new window]  and
Rebecca H. Hallett
Lauren E. Des Marteaux*
Affiliation:
Biology Center, Czech Academy of Sciences, Institute of Entomology, Branišovská 31, 370 05, České Budějovice, Czech Republic; School of Environmental Sciences, University of Guelph, 50 Stone Road East, Guelph, Ontario, N1G 2W1, Canada
Rebecca H. Hallett
Affiliation:
School of Environmental Sciences, University of Guelph, 50 Stone Road East, Guelph, Ontario, N1G 2W1, Canada
*
1Corresponding author (e-mail: ldesmart@gmail.com)
Get access Rights & Permissions [Opens in a new window]

Abstract

Larvae of the swede midge, Contarinia nasturtii (Kieffer) (Diptera: Cecidomyiidae), rely on environmental cues to initiate the diapause programme. This facultative diapause strategy, which provides opportunities for both bet hedging and multivoltinism, likely contributed to the successful colonisation and spread of this invasive pest in North America. Population diapause incidence is variable even under relatively stable conditions (especially at the critical day length), yet the mechanisms influencing the developmental trajectory of individuals under such conditions are unknown. Here we approach the non-environmental (i.e., heritable) controls of this variation by comparing diapause frequencies within and among full-sibling swede midge families reared in one of two stable environments. Under warm, long-day conditions > 99% of swede midges pupated directly, while 86% of swede midges entered diapause under cool, short-day conditions. In the latter condition, most families exhibited mixed developmental trajectories (ranging from 36% to 96% diapause). This developmental variation among siblings indicates that the diapause induction threshold does not follow simple Mendelian inheritance with complete dominance for a particular allele, but may follow incomplete dominance or a more complex heredity. Alternatively, within-family diapause variation may result from maternal bet hedging or factors such as maternal age or larval nutrition.

Type
Physiology, Biochemistry, Development, and Genetics
Information
The Canadian Entomologist , Volume 151 , Issue 4 , August 2019 , pp. 465 - 474
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

Subject editor: Hervé Colinet

References

Barnes, H.F. 1950. The identity of the swede midge, with notes on its biology. Annals of Applied Biology, 37: 241–248.CrossRefGoogle Scholar
Bergh, J., Harris, M., and Rose, S. 1992. Factors inducing mated behavior in female Hessian flies (Diptera: Cecidomyiidae). Annals of the Entomological Society of America, 85: 224–233.CrossRefGoogle Scholar
Blanckenhorn, W.U. and Heyland, A. 2005. The quantitative genetics of two life history trade-offs in the yellow dung fly in abundant and limited food environments. Evolutionary Ecology, 18: 385–402. https://doi.org/10.1007/s10682-004-2680-z.CrossRefGoogle Scholar
Boddum, T., Molnár, B.P., Hill, S.R., Birgersson, G.Å., Hansson, B.S., Abreha, K.B., et al. 2018. Host attraction and selection in the swede midge (Contarinia nasturtii). Frontiers in Ecology and Evolution, article 61, 1–9.Google Scholar
Boivin, T., Bouvier, J.-C., Beslay, D., and Sauphanor, B. 2004. Variability in diapause propensity within populations of a temperate insect species: interactions between insecticide resistance genes and photoperiodism. Biological Journal of the Linnean Society, 83: 341–351.CrossRefGoogle Scholar
Boyle, E.A., Li, Y.I., and Pritchard, J.K. 2017. An expanded view of complex traits: from polygenic to omnigenic. Cell, 169: 1177–1186. https://doi.org/10.1016/j.cell.2017.05.038.CrossRefGoogle ScholarPubMed
Bradford, M.J. and Roff, D.A. 1993. Bet hedging and the diapause strategies of the cricket Allonemobius fasciatus. Ecology, 74: 1129–1135.CrossRefGoogle Scholar
Chen, M. and Shelton, A.M. 2007. Impact of soil type, moisture, and depth on swede midge (Diptera: Cecidomyiidae) pupation and emergence. Environmental Entomology, 36: 1349–1355.CrossRefGoogle ScholarPubMed
Danks, H.V. 1987. Insect dormancy: an ecological perspective. Biological Survey of Canada, Ottawa, Ontario, Canada.Google Scholar
Denlinger, D.L. 2002. Regulation of diapause. Annual Review of Entomology, 47: 93–122.CrossRefGoogle ScholarPubMed
Denlinger, D.L. 2009. Diapause. In Encyclopedia of insects, second edition. Edited by Resh, V.H. and Cardé, R.T.. Elsevier, Burlington, Massachusetts, United States of America. Pp. 267–271.CrossRefGoogle Scholar
Des Marteaux, L.E., Habash, M.B., Schmidt, J.M., and Hallett, R.H. 2012. A method for induction and quantification of diapause entry in the swede midge (Diptera: Cecidomyiidae). The Canadian Entomologist, 144: 792–800.CrossRefGoogle Scholar
Des Marteaux, L.E., Schmidt, J.M., Habash, M.B., and Hallett, R.H. 2015. Patterns of diapause frequency and emergence in swede midges of southern Ontario. Agricultural and Forest Entomology, 17: 77–89.CrossRefGoogle Scholar
Dingle, H., Brown, C.K., and Hegmann, J.P. 1977. The nature of genetic variance influencing photoperiodic diapause in a migrant insect, Oncopeltus fasciatus. The American Naturalist, 111: 1047–1059.CrossRefGoogle Scholar
Emerson, K.J., Bradshaw, W.E., and Holzapfel, C.M. 2009. Complications of complexity: integrating environmental, genetic and hormonal control of insect diapause. Trends in Genetics, 25: 217–225.CrossRefGoogle ScholarPubMed
Ghalambor, C.K., McKay, J.K., Carroll, S.P., and Reznick, D.N. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology, 21: 394–407. https://doi.org/10.1111/j.1365-2435.2007.01283.x.CrossRefGoogle Scholar
Glass, E.H. 1969.Changes in diapause response to photoperiod in laboratory strains of Oriental fruit moth. Annals of the Entomological Society of America, 63: 74–76.CrossRefGoogle Scholar
Goto, S.G., Han, B., and Denlinger, D.L. 2006. A nondiapausing variant of the flesh fly, Sarcophaga bullata, that shows arrhythmic adult eclosion and elevated expression of two circadian clock genes, period and timeless. Journal of Insect Physiology, 52: 1213–1218.CrossRefGoogle ScholarPubMed
Hagstrum, D. and Silhacek, D. 1980. Diapause induction in Ephestia cautella: an interaction between genotype and crowding. Entomologia Experimentalis et Applicata, 28: 29–37.CrossRefGoogle Scholar
Hahn, D.A. and Denlinger, D.L. 2007. Meeting the energetic demands of insect diapause: nutrient storage and utilization. Journal of Insect Physiology, 53: 760–773.CrossRefGoogle ScholarPubMed
Hallett, R.H. 2017. The challenge of swede midge management in Canola. In Integrated management of insect pests on canola and other Brassica oilseed crops. Edited by Reddy, G.V.P.. Centre for Agriculture and Bioscience International, Boston, Massachusetts, United States of America. Pp. 44–67.CrossRefGoogle Scholar
Hallett, R.H., Goodfellow, S.A., Weiss, R.M., and Olfert, O. 2009. MidgEmerge, a new predictive tool, indicates the presence of multiple emergence phenotypes of the overwintered generation of swede midge. Entomologia Experimentalis et Applicata, 130: 81–97.CrossRefGoogle Scholar
Hallett, R.H. and Heal, J.D. 2001. First Nearctic record of the swede midge (Diptera: Cecidomyiidae), a pest of cruciferous crops from Europe. The Canadian Entomologist, 133: 713–715.CrossRefGoogle Scholar
Han, B. and Denlinger, D.L. 2009. Mendelian inheritance of pupal diapause in the flesh fly, Sarcophaga bullata. Journal of Heredity, 100: 251–255. https://doi.org/10.1093/jhered/esn082.CrossRefGoogle ScholarPubMed
Hand, S.C., Denlinger, D.L., Podrabsky, J.E., and Roy, R. 2016. Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish. American Journal of Physiology, 310: R1193–R1211.Google ScholarPubMed
Henrich, V.C. and Denlinger, D.L. 1983. Genetic differences in pupal diapause incidence between two selected strains of the flesh fly. Journal of Heredity, 74: 371–374.CrossRefGoogle Scholar
Hockham, L.R., Graves, J.A., and Ritchie, M.G. 2001. Variable maternal control of facultative egg diapause in the bushcricket Ephippiger ephippiger. Ecological Entomology, 26: 143–147. https://doi.org/10.1046/j.1365-2311.2001.00312.x.CrossRefGoogle Scholar
Hopper, K.R. 1999. Risk-spreading and bet-hedging in insect population biology. Annual Review of Entomology, 44: 535–560. https://doi.org/10.1146/annurev.ento.44.1.535.CrossRefGoogle ScholarPubMed
Hoy, M.A. 1978. Selection for a non-diapausing gypsy moth: some biological attributes of a new laboratory strain. Annals of the Entomological Society of America, 71: 75–80.CrossRefGoogle Scholar
Hunter, M.D. and McNeil, J.N. 1997. Host-plant quality influences diapause and voltinism in a polyphagous insect herbivore. Ecology, 78: 977–986.CrossRefGoogle Scholar
Kawakami, Y., Numata, H., Ito, K., and Goto, S.G. 2009. Dominant and recessive inheritance patterns of diapause in the two-spotted spider mite Tetranychus urticae. Journal of Heredity, 101: 20–25.CrossRefGoogle Scholar
Lynch, M. and Walsh, B. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, Massachusetts, United States of America.Google Scholar
Mahdjoub, T. and Menu, F. 2008. Prolonged diapause: a trait increasing invasion speed? Journal of Theoretical Biology, 251: 317–330.CrossRefGoogle ScholarPubMed
Marshall, D.J., Bonduriansky, R., and Bussière, L.F. 2008. Offspring size variation within broods as a bet-hedging strategy in unpredictable environments. Ecology, 89: 2506–2517. https://doi.org/10.1890/07-0267.1.CrossRefGoogle ScholarPubMed
Mathias, D., Jacky, L., Bradshaw, W.E., and Holzapfel, C.M. 2007. Quantitative trait loci associated with photoperiodic response and stage of diapause in the pitcher plant mosquito, Wyeomyia smithii. Genetics, 176: 391–402.CrossRefGoogle ScholarPubMed
Mori, A., Romero-Severson, J., and Severson, D. 2007. Genetic basis for reproductive diapause is correlated with life history traits within the Culex pipiens complex. Insect Molecular Biology, 16: 515–524.Google ScholarPubMed
Morris, R.F. and Fulton, W.C. 1970. Heritability of diapause intensity in Hyphantria cunea and correlated fitness responses. The Canadian Entomologist, 102: 927–938. https://doi.org/10.4039/Ent102927-8.CrossRefGoogle Scholar
Mousseau, T.A. 1991. Geographic variation in maternal-age effects on diapause in a cricket. Evolution, 45: 1053–1059.CrossRefGoogle Scholar
Nijhout, H.F. and Williams, C.M. 1974. Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): growth of the last-instar larva and the decision to pupate. Journal of Experimental Biology, 61: 481–491.Google ScholarPubMed
Poupardin, R., Schöttner, K., Korbelová, J., Provazník, J., Doležel, D., Pavlinic, D., et al. 2015. Early transcriptional events linked to induction of diapause revealed by RNAseq in larvae of drosophilid fly, Chymomyza costata. BMC Genomics, 16: 720.CrossRefGoogle ScholarPubMed
Rajon, E., Desouhant, E., Chevalier, M., Débias, F., and Menu, F. 2014. The evolution of bet hedging in response to local ecological conditions. The American Naturalist, 184: E1–E15.CrossRefGoogle ScholarPubMed
Ratcliff, W.C. and Denison, R.F. 2010. Individual-level bet hedging in the bacterium Sinorhizobium meliloti. Current Biology, 20: 1740–1744. https://doi.org/10.1016/j.cub.2010.08.036.CrossRefGoogle ScholarPubMed
Readshaw, J.L. 1961. The biology and ecology of the swede midge, Contarinia nasturtii (Kieffer) (Diptera: Cecidomyidae). Ph.D. thesis. University of Durham, Durham, United Kingdom.Google Scholar
Readshaw, J.L. 1966. The ecology of the swede midge, Contarinia nasturtii (Kieff.) (Diptera, Cecidomyiidae). I. Life-history and influence of temperature and moisture on development. Bulletin of Entomological Research, 56: 685–700.CrossRefGoogle Scholar
Reynolds, J., Bautista-Jimenez, R., and Denlinger, D. 2016. Changes in histone acetylation as potential mediators of pupal diapause in the flesh fly, Sarcophaga bullata. Insect Biochemistry and Molecular Biology, 76: 29–37.CrossRefGoogle ScholarPubMed
Reynolds, J.A., Clark, J., Diakoff, S.J., and Denlinger, D.L. 2013. Transcriptional evidence for small RNA regulation of pupal diapause in the flesh fly, Sarcophaga bullata. Insect Biochemistry and Molecular Biology, 43: 982–989.CrossRefGoogle ScholarPubMed
Reynolds, J.A., Peyton, J.T., and Denlinger, D.L. 2017. Changes in microRNA abundance may regulate diapause in the flesh fly, Sarcophaga bullata. Insect Biochemistry and Molecular Biology, 84: 1–14. https://doi.org/10.1016/j.ibmb.2017.03.002.CrossRefGoogle ScholarPubMed
Reznik, S.Y. and Samartsev, K.G. 2015. Multigenerational maternal inhibition of prepupal diapause in two Trichogramma species (Hymenoptera: Trichogrammatidae). Journal of Insect Physiology, 81: 14–20. https://doi.org/10.1016/j.jinsphys.2015.06.012.CrossRefGoogle Scholar
Roff, D.A. and Bradford, M.J. 2000. A quantitative genetic analysis of phenotypic plasticity of diapause induction in the cricket Allonemobius socius. Heredity, 84: 193–200.CrossRefGoogle ScholarPubMed
Rogerson, J.P. 1963. Swede midge on two Northumberland farms, 1959-61. Plant Pathology, 12: 161–171.CrossRefGoogle Scholar
Saunders, D.S. 1965. Larval diapause of maternal origin: induction of diapause in Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). Journal of Experimental Biology, 42: 495–508.Google Scholar
Saunders, D.S. 1987. Maternal influence on the incidence and duration of larval diapause in Calliphora vicina. Physiological Entomology, 12: 331–338.CrossRefGoogle Scholar
Sgro, C.M., Terblanche, J.S., and Hoffmann, A.A. 2016. What can plasticity contribute to insect responses to climate change? Annual Review of Entomology, 61: 433–451.CrossRefGoogle ScholarPubMed
Simons, A.M. and Johnston, M.O. 1997. Developmental instability as a bet-hedging strategy. Oikos, 80: 401–406.CrossRefGoogle Scholar
Smith, M.A.H., Wise, I.L., and Lamb, R.J. 2004. Sex ratios of Sitodiplosis mosellana (Diptera: Cecidomyiidae): implications for pest management in wheat (Poaceae). Bulletin of Entomological Research, 94: 569–575. https://doi.org/10.1079/BER2004333.CrossRefGoogle Scholar
Taylor, F. 1989. Diapause induction in changing photoperiods. Journal of Theoretical Biology, 139: 103–116.CrossRefGoogle Scholar
Timer, J., Tobin, P.C., and Saunders, M.C. 2010. Geographic variation in diapause induction: the grape berry moth (Lepidoptera: Tortricidae). Environmental Entomology, 39: 1751–1755. https://doi.org/10.1603/en10116.CrossRefGoogle Scholar
Togashi, K. 2017. Effects of crowding on larval diapause and adult body size in Monochamus alternatus alternatus (Coleoptera: Cerambycidae). The Canadian Entomologist, 149: 159–173.CrossRefGoogle Scholar
Waldbauer, G.P. and Sternburg, J.G. 1973. Polymorphic termination of diapause by Cecropia: genetic and geographical aspects. Biological Bulletin, 145: 627–641.CrossRefGoogle Scholar
Webster, A.K., Jordan, J.M., Hibshman, J.D., Chitrakar, R., and Baugh, L.R. 2018. Transgenerational effects of extended dauer diapause on starvation survival and gene expression plasticity in Caenorhabditis elegans. Genetics, 210: 263–274.CrossRefGoogle ScholarPubMed
Williams, K.D. and Sokolowski, M.B. 1993. Diapause in Drosophila melanogaster females: a genetic analysis. Heredity, 71: 312–317. https://doi.org/10.1038/hdy.1993.141.CrossRefGoogle ScholarPubMed
Winterhalter, W.E. and Mousseau, T.A. 2007. Patterns of phenotypic and genetic variation for the plasticity of diapause incidence. Evolution, 61: 1520–1531. https://doi.org/10.1111/j.1558-5646.2007.00127.x.CrossRefGoogle ScholarPubMed
Xu, W.-H., Sato, Y., Ikeda, M., and Yamashita, O. 1995. Stage-dependent and temperature-controlled expression of the gene encoding the precursor protein of diapause hormone and pheromone biosynthesis activating neuropeptide in the silkworm, Bombyx mori. Journal of Biological Chemistry, 270: 3804–3808. https://doi.org/10.1074/jbc.270.8.3804.CrossRefGoogle ScholarPubMed
Yamashita, O. 1996. Diapause hormone of the silkworm, Bombyx mori: structure, gene expression and function. Journal of Insect Physiology, 42: 669–679.CrossRefGoogle Scholar
Supplementary material: PDF

Des Marteaux and Hallett supplementary material

Des Marteaux and Hallett supplementary material 1

Download Des Marteaux and Hallett supplementary material(PDF)
PDF 103.4 KB