This Article Abstract Free Full Text (Free PDF) Free Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (14) Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Lankinen, P. Articles by Forsman, P. Search for Related Content PubMed PubMed Citation Articles by Lankinen, P. Articles by Forsman, P. Pubmed/NCBI databases Protein Compound via MeSH Substance via MeSH Social Bookmarking                         What's this?

Independence of Genetic Geographical Variation between Photoperiodic Diapause, Circadian Eclosion Rhythm, and Thr-Gly Repeat Region of the Period Gene in Drosophila littoralis

Department of Biology, University of Oulu, Oulu, Finland, pekka.lankinen{at}oulu.fi

P. Forsman

Department of Biology, University of Oulu, Oulu, Finland

Drosophila littoralis is a latitudinally widespread European species of the Drosophila virilis group. The species has ample genetic variation in photoperiodism (adult diapause) and circadian rhythmicity (pupal eclosion rhythm), with adaptive latitudinal clines in both of them. The possible common genetic basis between the variability of photoperiodism and circadian rhythms was studied by a long-term crossing experiment. A northern strain (65 °N) having long critical day length (CDL = 19.9 h) for diapause, early phase of the entrained rhythm in LD 3:21 (_LD3:21 = 12.3 h), and short period (= 18.8 h) of the free-running rhythm for the eclosion rhythm was crossed with a southern strain (42 °N) having short CDL (12.4 h), late eclosion phase (_LD3:21 = 20.2 h), and long period (= 22.8 h). After 54 generations, including free recombination, artificial selection, and genetic drift, a novel strain resulted, having even more "southern" diapause and more "northern" eclosion rhythm characteristics than found in any of the geographical strains. The observed complete separation of eclosion rhythm characteristics from photoperiodism is a new finding in D. littoralis; in earlier studies followed for 16 generations, the changes had been mostly parallel. Evidently, the genes controlling the variability of the eclosion rhythm and photoperiodism in D. littoralis are different but closely linked. To test for the possible gene loci underlying the observed geographical variability, the period gene was studied in 10 strains covering all the known clock variability in D. littoralis. The authors sequenced the most suspected Thr-Gly region, which is known to take part in the adaptive clock variability in Drosophila melanogaster. No coding differences were found in the strains, showing that this region is not included in the adaptive clock variability in D. littoralis.

Key Words: photoperiodism • diapause • circadian rhythm • period gene • latitudinal variation • Drosophila littoralis • clock genes

References

• Alexander ML (1976) The genetics of Drosophila virilis. In The Genetics and Biology of Drosophila, vol. 1c, Ashburner M and Novitski E, eds, pp 1365-1427, London, Academic Press.
• Allemand R and Boulétreau-Merle J (1989) Correlated responses in lines of Drosophila melanogaster selected for different oviposition behaviours. Experientia 45:1147-1150.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Ashmore LJ and Sehgal A (2003) A fly’s eye view of circadian entrainment. J Biol Rhythms 18:206-212.[Abstract/Free Full Text]
• Bollig I (1977) Different circadian rhythms regulate photoperiodic flowering response and leaf movement in Pharbitis nil (L.) Choisy. Planta 135:137-142.[CrossRef]
• Bradley HK and Saunders DS (1986) The selection for early and late pupariation in the flesh-fly, Sarcophaga argyrostoma, and its effect on the incidence of pupal diapause. Physiol Entomol 1:371-382.
• Bradshaw WE, Quebodeaux MC, and Holzapfel CM (2003) Circadian rhythmicity and photoperiodism in the pitcher-plant mosquito: Adaptive response to the photic environment or correlated response to the seasonal environment? Am Nat 161:735-748.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Bünning E (1936) Die endonome Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber Dtsch Bot Ges 54:590-607.
• Colot HV, Hall JC, and Rosbash M (1988) Interspecific comparison of the period gene of Drosophila reveals large blocks of non-conserved coding DNA. EMBO J 7:3929-3937.[Web of Science][Medline] [Order article via Infotrieve]
• Costa R and Kyriacou CP (1998) Functional and evolutional implications of natural variation in clock genes. Curr Opin Neurobiol 8:659-664.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Danilevskii AS (1965) Photoperiodism and Seasonal Development in Insects. Edinburgh, UK: Oliver & Boyd.
• Enright JT (1965) The search of rhythmicity in biological time-series. J Theor Biol 8:426-468.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Hilton H and Hey J (1996) DNA sequence variation at the period locus reveals the history and speciation event in the Drosophila virilis group. Genetics 144:1015-1025.[Abstract]
• Lankinen P (1982) The inheritance of pupal eclosion rhythm in Drosophila littoralis. Hereditas 97:324-325.
• Lankinen P (1985) Genetic Variation of Circadian Eclosion Rhythm, and Its Relation to Photoperiodism in Drosophila littoralis. Doctoral dissertation, University of Oulu, Oulu.
• Lankinen P (1986a) Geographical variation in circadian eclosion rhythm and photoperiodic adult diapause in Drosophila littoralis. J Comp Physiol A 159:123-142.[CrossRef]
• Lankinen P (1986b) Genetic correlation between circadian eclosion rhythm and photoperiodic diapause in Drosophila littoralis. J Biol Rhythms 1:101-118.[Abstract/Free Full Text]
• Lankinen P (1993) North-south differences in circadian eclosion rhythm in European populations of Drosophila subobscura. Heredity 71:210-218.[CrossRef][Web of Science]
• Lankinen P and Lumme J (1982) An improved apparatus for recording the eclosion rhythm in Drosophila. Dros Inf Serv 58:161-163.
• Lankinen P and Lumme J (1984) Genetic analysis of geographic variation in photoperiodic diapause and pupal eclosion rhythm in Drosophila littoralis. In Photoperiodic Regulation of Insect and Molluscan Hormones, Ciba Foundation Symposium No. 104, Porter R and Collins GM, eds, pp 97-117, London, Pitman.
• Lumme J and Oikarinen A (1977) The genetic basis of the geographically variable photoperiodic diapause in Drosophila littoralis. Hereditas 86:129-142.[CrossRef][Web of Science]
• Lumme J and Pohjola L (1980) Selection against photoperiodic diapause started from monohybrid crosses in Drosophila littoralis. Hereditas 91:377-338.
• Majercak J, Sidote D, Hardin PE, and Edery I (1999) How a circadian clock adapts to seasonal decreases in temperature and day length. Neuron 24:219-230.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Nielsen J, Peixoto AA, Piccin A, Costa R, Kyriacou CP, and Chalmers D (1994) Big flies, small repeats: The "Thr-Gly" region of the periodgene in Diptera. Mol Biol Evol 11:839-853.[Abstract]
• Patterson JT and Stone WS (1952) Evolution in the Genus Drosophila. New York: Macmillan.
• Pittendrigh CS (1966) The circadian oscillation in Drosophila pseudoobscura pupae: A model for the photoperiodic clock. Z Pflanzenphysiol Bd 54:275-307.
• Pittendrigh CS, Elliot J, and Takamura T (1984) The circadian component in photoperiodic induction. In Photoperiodic Regulation of Insect and Molluscan Hormones, Ciba Foundation Symposium No. 104, Porter R and Collins GM, eds, pp 26-47, London, Pitman.
• Pittendrigh CS and Minis DH (1971) The photoperiodic measurement in Pectinophora gossypiella and its relation to the circadian system in that species. In Biochronometry, Menaker M, ed, pp 212-250, Washington, DC, National Academy in Sciences.
• Possidente BP and Hegmann JP (1980) Circadian complexes under common gene control. J Comp Physiol B 139:121-125.
• Riihimaa A (1996) Genetic variation in diapause, cold hardiness and circadian eclosion rhythm in Chymomyza costata. Acta Universitatis Ouluensis A 274:1-60.
• Saunders DS (1990) The circadian basis of ovarian diapause regulation in Drosophila melanogaster: Is the period gene causally involved in photoperiodic time measurement? J Biol Rhythms 5:315-331.[Abstract/Free Full Text]
• Saunders DS and Cymborowski B (2003) Selection for high diapause incidence in blow flies (Calliphora vicina) maintained under long days increases the maternal critical daylength: Some consequences for the photoperiodic clock. J Insect Physiol 49:777-784.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Saunders DS, Henrich VC, and 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.[Abstract/Free Full Text]
• Sawyer LA, Hennessy JM, Peixoto AA, Rosato E, Parkinson H, Costa R, and Kyriacou CP (1997) Natural variation in a Drosophila clock gene and temperature compensation. Science 278:2117-2120.[Abstract/Free Full Text]
• Tauber E and Kyriacou BP (2001) Insect photoperiodism and circadian clocks: Models and mechanisms. J Biol Rhythms 16:381-390.[Abstract/Free Full Text]
• Tei H, Okamura H, Shigeyoshi Y, Fukuhara C, Ozawa R, Hirose M, and Sakagi Y (1997) Circadian oscillation of a mammalian homologue of the Drosophila period gene. Nature 38:512-516.
• Vaz Nunes M and Saunders D (1999) Photoperiodic time measurement in insects: A review of clock models. J Biol Rhythms 14:84-104.[Abstract/Free Full Text]
• Veerman A (2001) Photoperiodic time measurement in insects and mites: A critical evaluation of the oscillator-clock hypothesis. J Insect Physiol 47:1097-1109.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Veerman A and Veenendaal RL (2003) Experimental evidence for a non-clock role of the circadian system in spider mite photoperiodism. J Insect Physiol 49:727-732.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]

Journal of Biological Rhythms, Vol. 21, No. 1, 3-12 (2006)
DOI: 10.1177/0748730405283418


CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				T. Sakamoto, O. Uryu, and K. Tomioka The Clock Gene period Plays an Essential Role in Photoperiodic Control of Nymphal Development in the Cricket Modicogryllus siamensis J Biol Rhythms, October 1, 2009; 24(5): 379 - 390. [Abstract] [PDF]

				B. Han and D. L. Denlinger Mendelian Inheritance of Pupal Diapause in the Flesh Fly, Sarcophaga bullata J. Hered., March 1, 2009; 100(2): 251 - 255. [Abstract] [Full Text] [PDF]

This Article Abstract Free Full Text (Free PDF) Free Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (14) Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Lankinen, P. Articles by Forsman, P. Search for Related Content PubMed PubMed Citation Articles by Lankinen, P. Articles by Forsman, P. Pubmed/NCBI databases Protein Compound via MeSH Substance via MeSH Social Bookmarking                         What's this?