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Adult reproductive diapause in Drosophila suzukii females

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Abstract

Drosophila suzukii (Diptera: Drosophilidae) is an emerging pest of soft fruits, but in this species diapause has not been thoroughly explored. We examined the effects of different temperatures and photoperiods on diapause induction and termination under laboratory conditions. There was variation in the ovarian development and oviposition rate under different photoperiods at 10 ± 1 °C, and the percentage of adults with immature ovaries was higher during the short photoperiod (8L:16D) than other photoperiods at 10 ± 1 °C. Adults were most sensitive to photoperiod within 3 days of eclosion. The optimal combination of photoperiod and temperature for diapause termination was a long photoperiod (16L:8D) at 25 ± 1 °C. The supercooling point was significantly reduced in reproductive diapause females, and trehalase, pyruvate kinase, sorbitol dehydrogenase, hexokinase and phosphofructokinase enzyme activities were significantly reduced (36.46, 57.85, 32.64, 54.68 and 24.59 %, respectively); glycogen and triglyceride levels were significantly increased (42.17 and 120.36 %). We conclude that D. suzukii is typical of short-day diapause species within a certain photoperiod range. This information might contribute to a more fundamental understanding of adult reproductive diapause for this important pest.

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References

  • Allen MJ (2007) What makes a fly enter diapause? Fly (Austin) 1(6):307–310

    Article  Google Scholar 

  • Asplen MK, Anfora G, Biondi A, Choi DS, Chu D, Daane KM et al (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494

    Article  Google Scholar 

  • Baker DA, Russell S (2009) Gene expression during Drosophila melanogaster egg development before and after reproductive diapause. BMC Genomics 24:242

    Article  Google Scholar 

  • Beck SD (1980) Insect photoperiodism, 2nd edn. Academic Press, New York, pp 119–185

    Google Scholar 

  • Calabria G, Maca J, Bachli G, Serra L, Pascual M (2012) First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136:139–147

    Article  Google Scholar 

  • Carson HL, Stalker HD (1948) Reproductive diapause in Drosophila Robusta. Proc Natl Acad Sci USA 34(3):124–129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chabert S, Allemand R, Poyet M, Eslin P, Gibert P (2012) Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii. Biol Control 63:40–47

    Article  Google Scholar 

  • Chen CP, Walker VK (1994) Cold-shock and chilling tolerance in Drosophila. J Insect Physiol 40:661–669

    Article  Google Scholar 

  • Cini A, Anfora G, Escudero-Colomar LA, Grassi A, Santosuosso U, Seljak G, Papini A (2014) Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. J Pest Sci 87:559–566

    Article  Google Scholar 

  • Daane KM, Wang XG, Biondi A, Miller B, Miller JC et al (2016) First exploration of parasitoids of Drosophila suzukii in South Korea as potential classical biological agents. J Pest Sci. doi:10.1007/s10340-016-0740-0

    Google Scholar 

  • Dalton DT, Walton VM, Shearer PW, Walsh DB, Caprile J, Isaacs R (2011) Laboratory survival of Drosophila suzukii under simulated winter conditions of the Pacific Northwest and seasonal field trapping in five primary regions of small and stone fruit production in the United States. Pest Manag Sci 67(11):1368–1374

    Article  CAS  PubMed  Google Scholar 

  • Denlinger DL (2002) Regulation of diapause. Annu Rev Entomol 47:93–122

    Article  CAS  PubMed  Google Scholar 

  • Denlinger DL (2008) Why study diapause? Entomol Res 38:1–9

    Article  Google Scholar 

  • Deprá M, Poppe JL, Schmitz HJ, De Toni DC, Valente VLS (2014) The first records of the invasive pest Drosophila suzukii in the South American continent. J Pest Sci 87(3):379–383

    Article  Google Scholar 

  • Formby JP, Krishnan N, Riggins JJ (2013) Supercooling in the Redbay Ambrosia Beetle (Coleoptera: Curculionidae). Fla Entomol 96(4):1530–1540

    Article  Google Scholar 

  • Guo HB, Xu YY, Ju Z, Li MG (2006) Seasonal changes of cold hardiness of the green lacewing, Chrysoperla sinica (Tjeder) (Neuroptera:Chrysopidae). Acta Ecol Sin 26(10):3238–3244

    Google Scholar 

  • Haye T, Girod P, Cuthbertson AGS, Wang XG, Daane KM, Hoelmer KA et al (2016) Current SWD IPM tactics and their practical implementation in fruit crops across different regions around the world. J Pest Sci. doi:10.1007/s10340-016-0737-8

    Google Scholar 

  • Hodek I, Hodkov M (1988) Multiple role of temperature during insect diapause. A review. Entomol Exp Appl 49:153–166

    Article  Google Scholar 

  • Jakobs R, Gariepy TD, Sinclair BJ (2015) Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii. J Insect Physiol 79:1–9

    Article  CAS  PubMed  Google Scholar 

  • Jiang XF, Huang SH, Luo LZ, Liu Y, Zhang L (2010) Diapause termination, post-diapause development and reproduction in the beet webworm, Loxostege sticticalis (Lepidoptera: Pyralidae). J Insect Physiol 56:1325–1331

    Article  CAS  PubMed  Google Scholar 

  • Kamei Y, Hasegawa Y, Niimi T, Yamashita O, Yaginuma T (2011) Trehalase-2 protein contributes to trehalase activity enhanced by diapause hormone in developing ovaries of the silkworm, Bombyx mori. J Insect Physiol 57:608–613

    Article  CAS  PubMed  Google Scholar 

  • Kankare M, Salminen T, Laiho A, Vesala L, Hoikkala A (2010) Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: a candidate gene microarray study. BMC Ecol 10:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanzawa T (1936) Studies on Drosophila suzukii mats. J Plant Prot (Tokyo) 23:66–70

    Google Scholar 

  • Kanzawa T (1939) Studies on Drosophila suzukii mats. Kofu. Yamanashi Agricultural Experimental Station, Yamanashi, pp 1–49

    Google Scholar 

  • Kelty JD, Lee RE Jr (2001) Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophilidae) during ecologically based thermoperiodic cycles. J Exp Biol 204:1659–1666

    CAS  PubMed  Google Scholar 

  • Kimura MT (2004) Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia 140:442–449

    Article  PubMed  Google Scholar 

  • King RC (1970) Ovarian development in Drosophila melanogaster. Academic, New York

    Google Scholar 

  • Kobayashi N, Takahashi M, Kihara S, Niimi T, Yamashita O, Yaginuma T (2014) Cloning of cDNA encoding a Bombyx mori homolog of human oxidation resistance 1 (OXR1) protein from diapause eggs, and analyses of its expression and function. J Insect Physiol 68:58–68

    Article  CAS  PubMed  Google Scholar 

  • Kondo M, Kimura MT (2008) Diversity of drosophilid Flies on Kume-jima, a subtropical island: comparison with diversity on Iriomote-jima. Entomol Sci 11:7–15

    Article  Google Scholar 

  • Kubrak OI, Kučerová L, Theopold U, Nässel DR (2014) The sleeping beauty: how reproductive diapause affects hormone signaling, metabolism, immune response and somatic maintenance in Drosophila melanogaster. PLoS ONE 9(11):e113051

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin QC, Zhai YF, Zhou CG, Li LL, Zhuang QY, Zhang XY et al (2014a) Behavioral rhythms of Drosophila suzukii and Drosoplia melanogaster. Fla Entomol 97(4):1424–1433

    Article  Google Scholar 

  • Lin QC, Zhai YF, Zhang AS, Men XY, Zhang XY, Zalom FG et al (2014b) Comparative developmental times and laboratory life tables for Drosophila suzukii and Drosophila melanogaster. Fla Entomol 97(4):1434–1442

    Article  Google Scholar 

  • Liu Z, Gong P, Li D, Wei W (2010) Pupal diapause of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) mediated by larval host plants: pupal weight is important. J Insect Physiol 56:1863–1870

    Article  CAS  PubMed  Google Scholar 

  • Lumme J, Oikarinen A, Lakovaara S, Alatalo R (1973) The environmental regulation of adult diapause in Drosophila littoralis. J Insect Physiol 20(10):2023–2033

    Article  Google Scholar 

  • MacMillan HA, Guglielmo CG, Sinclair BJ (2009) Membrane remodeling and glucose in Drosophila melanogaster: a test of rapid cold-hardening and chilling tolerance hypotheses. J Insect Physiol 55:243–249

    Article  CAS  PubMed  Google Scholar 

  • Mitsui H, Beppu K, Kimura MT (2010) Seasonal life cycles and resource uses of flower- and fruit-feeding drosophilid flies (Diptera: Drosophilidae) in central Japan. Entomol Sci 13:60–67

    Article  Google Scholar 

  • Murphy KA, West JD, Kwok RS, Chiu JC (2016) Accelerating research on Spotted Wing Drosophila management using genomic technologies. J Pest Sci. doi:10.1007/s10340-016-0741-z

    Google Scholar 

  • Nyamukondiwa C, Terblanche JS, Marshall KE, Sinclair BJ (2011) Basal cold but not heat tolerance constrains plasticity among Drosophila species (Diptera: Drosophilidae). J Evol Biol 24:1927–1938

    Article  CAS  PubMed  Google Scholar 

  • 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(1):720

    Article  PubMed  PubMed Central  Google Scholar 

  • Rider MH, Hussain N, Dilworth SM, Storey JM, Storey KB (2011) AMP-activated protein kinase and metabolic regulation in cold-hardy insects. J Insect Physiol 57:1453–1462

    Article  CAS  PubMed  Google Scholar 

  • Rossi-Stacconi MV, Kaur R, Mazzoni V, Ometto L, Grassi A, Gottardello A et al (2016) Multiple lines of evidence for reproductive winter diapause in the invasive pest Drosophila suzukii: useful clues or control strategies. J Pest Sci. doi:10.1007/s10340-016-0753-8

    Google Scholar 

  • Rota-Stabelli O, Blaxter M, Anfora G (2013) Drosophila suzukii. Curr Biol 23:R8–R9

    Article  CAS  PubMed  Google Scholar 

  • Rozsypal J, Koštál V, Zahradníčková H, Šimek P (2013) Overwintering strategy and mechanisms of cold tolerance in the codling moth (Cydia pomonella). PLoS ONE 8(4):e61745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubio RO, Suzuki A, Mitsumasu K, Homma T, Niimi T, Yamashita O, Yaginuma T (2011) Cloning of cDNAs encoding sorbitol dehydrogenase-2a and b, enzymatic characterization, and up-regulated expression of the genes in Bombyx mori diapause eggs exposed to 5°C. Insect Biochem Mol Biol 41:378–387

    Article  CAS  PubMed  Google Scholar 

  • Salminen TS, Hoikkala A (2013) Effect of temperature on the duration of sensitive period and on the number of photoperiodic cycles required for the induction of reproductive diapause in Drosophila montana. J Insect Physiol 59(4):450–457

    Article  CAS  PubMed  Google Scholar 

  • Schmidt PS, Zhu CT, Das J, Batavia M, Yang L, Eanes WF (2008) An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster. Proc Natl Acad Sci USA 105(42):16207–16211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spieth HR (1995) Change in photoperiodic sensitivity during larval development of Pieris brassicae. J Insect Physiol 41:77–83

    Article  CAS  Google Scholar 

  • Stephens AR, Asplen MK, Hutchison WD, Venette RC (2015) Cold hardiness of winter-acclimated Drosophila suzukii (Diptera: Drosophilidae) adults. Environ Entomol 44(6):1619–1626

    Article  CAS  PubMed  Google Scholar 

  • Walsh DB, Bolda MP, Goodhue RE, Dreves AJ, Lee JC (2010) Drosophila suzukii (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding its geographic range and damage potential. J Integr Pest Manag 2:G1–G7

    Article  Google Scholar 

  • Wang XG, Stewart TJ, Biondi A, Chavez BA, Ingels C, Caprile J et al (2016) Population dynamics and ecology of Drosophila suzukii in Central California. J Pest Sci. doi:10.1007/s10340-016-0747-6

    Google Scholar 

  • Williams KD, Busto M, Suster ML, So AK, Ben-Shahar Y, Leevers SJ, Sokolowski MB (2006) Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase. Proc Natl Acad Sci USA 103(43):15911–15915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao L, Fu S, Xue FS (2013) Characters of insect diapause stage and photoperiod sensitive stage. Biol Disaster Sci 36:1–8 (in Chinese)

    Google Scholar 

  • Xue FS, Spieth HR, Li AQ, Hua A (2002) The role of photoperiod and temperature in determination of summer and winter diapause in the cabbage beetle, Colaphellus bowringi (Coleoptera: Chrysomelidae). J Insect Physiol 48:279–2861

    Article  CAS  PubMed  Google Scholar 

  • Yamada H, Yamamoto MT (2011) Association between circadian clock genes and diapause incidence in Drosophila triauraria. PLoS ONE 6(12):e27493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zerulla FN, Schmidt S, Streitberger M, Zebitz CPW, Zelger R (2015) On the overwintering ability of Drosophila suzukii in South Tyrol. J Berry Res 5:41–48

    Google Scholar 

  • Zhai YF, Lin QC, Zhou XH, Zhang XY, Liu TL, Yu Y (2014) Identification and validation of reference genes for quantitative real-time PCR in Drosophila suzukii (Diptera: Drosophilidae). PLoS ONE 9(9):e106800

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou Z, Li Y, Yuan C, Zhang Y, Qu L (2015) Oral administration of TAT-PTD-DIAPAUSE hormone fusion protein interferes with Helicoverpa armigera (Lepidoptera: Noctuidae) development. J Insect Sci 28:15

    CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported through a grant from the Shandong Provincial Natural Science Foundation, China (ZR2014CQ014), and the National Natural Science Foundation of China (31401803). The authors wish to thanks Jianlong Bi for the manuscript language revision.

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Authors and Affiliations

  1. Institute of Plant Protection, Shandong Academy of Agricultural Sciences, Jinan, 250100, China

    Yifan Zhai, Qingcai Lin, Li Zheng & Yi Yu

  2. MoA-CABI Joint Laboratory for Bio-Safety, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, 100193, China

    Jinping Zhang & Feng Zhang

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  1. Yifan Zhai
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  2. Qingcai Lin
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  3. Jinping Zhang
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  4. Feng Zhang
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Correspondence to Yifan Zhai or Yi Yu.

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Communicated by A. Biondi.

Special Issue: Spotted Wing Drosophila.

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Zhai, Y., Lin, Q., Zhang, J. et al. Adult reproductive diapause in Drosophila suzukii females. J Pest Sci 89, 679–688 (2016). https://doi.org/10.1007/s10340-016-0760-9

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