Abstract
Drosophila melanogaster from Australia, Europe and North America enter an adult ovarian dormancy in response to short days and low temperatures. The independent effects of temperature and day length in the determination of dormancy have been examined only in one long-established laboratory line (Canton-S). In all other studies of natural or laboratory populations, dormancy has been assessed at either a single short day or a single moderately low temperature. Herein, we determine the relative roles of temperature, photoperiod, and their interaction in the control of ovarian dormancy in D. melanogaster from two natural populations representing latitudinal extremes in eastern North America (Florida at 27°N and Maine at 44°N). In both natural populations, temperature is the main determinant of dormancy, alone explaining 67% of the total variation among replicate isofemale lines, whereas photoperiod has no significant effect. We conclude that ovarian dormancy in D. melanogaster is a temperature-initiated syndrome of winter-tolerant traits that represents an adaptive phenotypic plasticity in temperate seasonal environments.
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Abbreviations
- L:D:
-
Number of hours of light (L) and dark (D) in a given environmental cycle
References
Bradshaw WE, Lounibos LP (1977) Evolution of dormancy and its photoperiodic control in pitcher-plant mosquitoes. Evolution 31:546–567
Bridges CB, Brehme KS (1944) The mutants of Drosophila melanogaster. Carnegie Institution of Washington, Washington
Danks HV (1987) Insect dormancy: an ecological perspective. Biological Survey of Canada (Terrestrial Arthropods), Ottawa
David JR, Capy P (1988) Genetic variation of Drosophila melanogaster natural populations. Trends Genet 4:106–111
Denlinger DL (1986) Dormancy in tropical insects. Annu Rev Entomol 31:239–264
Hoffmann AA, Scott M, Partridge L, Hallas R (2003) Overwintering in Drosophila melanogaster: outdoor field cage experiments on clinal and laboratory selected populations help to elucidate traits under selection. J Evol Biol 16:614–623
Kimura MT (1984) Geographic variation of reproductive diapause in the Drosophila auraria complex (Diptera, Drosophilidae). Physiol Entomol 9:425–431
King RC (1970) Ovarian development in Drosophila melanogaster. Academic Press, New York
Lankinen P (1986) Geographical variation in circadian eclosion rhythm and photoperiodic adult diapause in Drosophila littoralis. J Comp Phys A 159:123–142
Leather SR, Walters KFA, Bale JS (1993) The ecology of insect overwintering. Cambridge University Press, Cambridge
R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Richard DS, Watkins NL, Serafin RB, Gilbert LI (1998) Ecdysteroids regulate yolk protein uptake by Drosophila melanogaster oocytes. J Insect Physiol 44:637–644
Saunders DS, Gilbert LI (1990) Regulation of ovarian diapause in Drosophila melanogaster by photoperiod and moderately low temperature. J Insect Physiol 36:195–200
Saunders DS, Henrich VC, Gilbert LI (1989) Induction of diapause in Drosophila melanogaster: photoperiodic regulation and the impact of arrhythmic clock mutations on time measurement. Proc Natl Acad Sci USA 86:3748–3752
Schmidt PS, Conde DR (2006) Environmental heterogeneity and the maintenance of genetic variation for reproductive diapause in Drosophila melanogaster. Evolution 60:1602–1611
Schmidt PS, Matzkin L, Ippolito M, Eanes WF (2005a) Geographic variation in diapause incidence, life-history traits, and climatic adaptation in Drosophila melanogaster. Evolution 59:1721–1732
Schmidt PS, Paaby AB, Heschel MS (2005b) Genetic variance for diapause expression and associated life histories in Drosophila melanogaster. Evolution 59:2616–2625
Tatar M, Chien SA, Priest NK (2001) Negligible senescence during reproductive dormancy in Drosophila melanogaster. Am Nat 158:248–258
Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, New York
Tauber E, Zordan M, Sandrelli F, Pegoraro M, Osterwalder N, Breda C, Daga A, Selmin A, Monger K, Benna C, Rosato E, Kyriacou CP, Costa R (2007) Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316:1895–1898
Williams KD, Sokolowski MB (1993) Diapause in Drosophila melanogaster females: a genetic analysis. Heredity 71:312–317
Williams KD, Busto M, Suster ML, So AKC, 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 103:15911–15915
Acknowledgments
We thank V. Koštál, and E. Tauber for discussion and for comments on previous versions of this paper, and L. Sherson and K. Kim for participation in the early stages of this research. J. Giebultowicz graciously supplied our Canton-S line. All work presented here complied with the “Principles of animal care”, publication No. 86-23 of the National Institute of Health, and also with current laws of the United States, where these experiment were performed. This work was made possible by generous support from the National Science Foundation through grants DEB-0412573 and IOB-0445710 to WEB, grant DEB-0542859 to PSS, and the National Science Foundation IGERT Training program grant DGE-0504727 to KJE.
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Emerson, K.J., Uyemura, A.M., McDaniel, K.L. et al. Environmental control of ovarian dormancy in natural populations of Drosophila melanogaster . J Comp Physiol A 195, 825–829 (2009). https://doi.org/10.1007/s00359-009-0460-5
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DOI: https://doi.org/10.1007/s00359-009-0460-5