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Applied Entomology and Zoology

, Volume 51, Issue 4, pp 515–520 | Cite as

Intraspecific variation in heat tolerance of Drosophila prolongata (Diptera: Drosophilidae)

  • Yurika Hitoshi
  • Yukio Ishikawa
  • Takashi MatsuoEmail author
Original Research Paper

Abstract

Tolerance to extreme temperatures is one of the most important components of adaptation to environments in insects. However, the genetic mechanisms of tolerance to long-term heat stress are mostly unknown. In this study, we investigated the genetic variation of susceptibility to long-term heat stress among the isofemale strains of Drosophila prolongata Singh & Gupta. High rates of pupal lethality were observed at 25 °C, showing that D. prolongata is more susceptible to heat stress than other Drosophila species. Susceptibility to heat stress was significantly different among the isofemale strains, suggesting that intraspecific genetic variation is involved in the reduced heat tolerance of D. prolongata. Unexpectedly, the tertiary sex ratio was biased to females at temperatures higher than 20 °C, indicating that the males were more susceptible to heat stress. These results demonstrated that D. prolongata is useful for genetic analysis for elucidating the molecular mechanisms of heat tolerance in insects.

Keywords

Long-term heat stress Heat-induced lethality Genetic variation Drosophila prolongata Sex ratio 

Notes

Acknowledgments

This work was supported by JSPS KAKENHI Grant Number 26660263 to TM.

References

  1. Bettencourt BR, Feder ME (2001) Hsp70 duplication in the Drosophila melanogaster species group: how and when did two become five? Mol Biol Evol 18(7):1272–1282. doi: 10.1093/oxfordjournals.molbev.a003912 CrossRefPubMedGoogle Scholar
  2. Calabria G, Dolgova O, Rego C, Castaneda LE, Rezende EL, Balanya J, Pascual M, Sorensen JG, Loeschcke V, Santos M (2012) Hsp70 protein levels and thermotolerance in Drosophila subobscura: a reassessment of the thermal co-adaptation hypothesis. J Evol Biol 25(4):691–700. doi: 10.1111/j.1420-9101.2012.02463.x CrossRefPubMedGoogle Scholar
  3. Chen H, Xu XL, Li YP, Wu JX (2014) Characterization of heat shock protein 90, 70 and their transcriptional expression patterns on high temperature in adult of Grapholita molesta (Busck). Insect Sci 21(4):439–448. doi: 10.1111/1744-7917.12057 CrossRefPubMedGoogle Scholar
  4. Crosthwaite JC, Sobek S, Lyons DB, Bernards MA, Sinclair BJ (2011) The overwintering physiology of the emerald ash borer, Agrilus planipennis fairmaire (Coleoptera: Buprestidae). J Insect Physiol 57(1):166–173. doi: 10.1016/j.jinsphys.2010.11.003 CrossRefPubMedGoogle Scholar
  5. Dobzhansky T (1935) Fecundity in Drosophila pseudoobscura at different temperatures. J Exp Zool 71:449–464CrossRefGoogle Scholar
  6. Hurst GDD, Johnson AP, von der Schulenburg JHG, Fuyama Y (2000) Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156(2):699–709PubMedPubMedCentralGoogle Scholar
  7. Ichiki R, Takasu K, Shima H (2003) Effects of temperature on immature development of the parasitic fly Bessa parallela (Meigen) (Diptera: Tachinidae). Appl Entomol Zool 38(4):435–439. doi: 10.1303/aez.2003.435 CrossRefGoogle Scholar
  8. Kellermann V, Overgaard J, Hoffmann AA, Flojgaard C, Svenning JC, Loeschcke V (2012) Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically. Proc Natl Acad Sci USA 109(40):16228–16233. doi: 10.1073/pnas.1207553109 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Kudo A, Takamori H, Watabe H, Ishikawa Y, Matsuo T (2015) Variation in morphological and behavioral traits among isofemale strains of Drosophila prolongata (Diptera: Drosophilidae). Entomol Sci 18(2):221–229. doi: 10.1111/ens.12116 CrossRefGoogle Scholar
  10. Moiroux J, Brodeur J, Boivin G (2014) Sex ratio variations with temperature in an egg parasitoid: behavioural adjustment and physiological constraint. Anim Behav 91:61–66. doi: 10.1016/j.anbehav.2014.02.021 CrossRefGoogle Scholar
  11. Omkar, Pervez A (2004) Temperature-dependent development and immature survival of an aphidophagous ladybeetle Propylea dissecta (Mulsant). J Appl Entomol 128(7):510–514. doi: 10.1111/j.1439-0418.2004.00881.510-514 CrossRefGoogle Scholar
  12. Pakyari H, Fathipour Y, Enkegaard A (2011) Effect of temperature on life table parameters of predatory thrips Scolothrips longicornis (Thysanoptera: Thripidae) fed on twospotted spider mites (Acari: Tetranychidae). J Econ Entomol 104(3):799–805. doi: 10.1603/EC10144 CrossRefPubMedGoogle Scholar
  13. Parsell DA, Lindquist S (1993) The function of heat-shock proteins in stress tolerance—degradation and reactivation of damaged proteins. Annu Rev Genet 27:437–496. doi: 10.1146/annurev.ge.27.120193.002253 CrossRefPubMedGoogle Scholar
  14. Petavy G, David JR, Gibert P, Moreteau B (2001) Viability and rate of development at different temperatures in Drosophila: a comparison of constant and alternating thermal regimes. J Therm Biol 26(1):29–39. doi: 10.1016/S0306-4565(00)00022-X CrossRefPubMedGoogle Scholar
  15. R Development Core Team (2008) R: a language and environment for statistical computing. R foundation for statistical computing, vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org
  16. Singh BK, Gupta JP (1977) Two new and two unrecorded species of the genus Drosophila fallen (Diptera: Drosophilidae) from Shillong, Meghalaya, India. Proc Zool Soc 30:31–38Google Scholar
  17. Takahashi KH, Okada Y, Teramura K (2011) Genome-wide deficiency screen for the genomic regions responsible for heat resistance in Drosophila melanogaster. BMC Genet 12:57. doi: 10.1186/1471-2156-12-57 PubMedPubMedCentralGoogle Scholar
  18. Toda MJ (1991) Drosophilidae (Diptera) in Myanmar (Burma) VII. The Drosophila melanogaster species-group, excepting the D. montium species-subgroup. Orient Insects 25:69–94CrossRefGoogle Scholar
  19. Tungjitwitayakul J, Tatun N, Vajarasathira B, Sakurai S (2015) Expression of heat shock protein genes in different developmental stages and after temperature stress in the maize weevil (Coleoptera: Curculionidae). J Econ Entomol 108(3):1313–1323. doi: 10.1093/jee/tov051 CrossRefPubMedGoogle Scholar
  20. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6(10):741–751. doi: 10.1038/nrmicro1969 CrossRefPubMedGoogle Scholar
  21. Wharton DA (2011) Cold tolerance of New Zealand alpine insects. J Insect Physiol 57(8):1090–1095. doi: 10.1016/j.jinsphys.2011.03.004 CrossRefPubMedGoogle Scholar

Copyright information

© The Japanese Society of Applied Entomology and Zoology 2016

Authors and Affiliations

  • Yurika Hitoshi
    • 1
  • Yukio Ishikawa
    • 1
  • Takashi Matsuo
    • 1
    Email author
  1. 1.Department of Agricultural and Environmental BiologyThe University of TokyoBunkyo-KuJapan

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