Latitudinal clines: An evolutionary view on biological rhythms

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1765, 2013, Pages

  Hut, Roelof A ^a   Paolucci, Silvia ^a   Dor, Roi ^b   Kyriacou, Charalambos P ^c   Daan, Serge ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b TEL AVIV UNIVERSITY   (Israel)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Circadian; Circannual; Diapause; Latitude; Photoperiod; Reproduction

Indexed keywords

ANNUAL CYCLE; BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; CLINE; EVOLUTIONARY BIOLOGY; LATITUDE; PHENOTYPE;

ALTITUDE; ANIMAL; BIOLOGICAL RHYTHM; CIRCADIAN RHYTHM; EVOLUTION; GENETIC POLYMORPHISM; GENETICS; INSECT; PHOTOPERIODICITY; PHYSIOLOGY; SEASON; VERTEBRATE;

ALTITUDE; ANIMALS; BIOLOGICAL CLOCKS; BIOLOGICAL EVOLUTION; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; INSECTS; PHOTOPERIOD; POLYMORPHISM, GENETIC; SEASONS; VERTEBRATES;

EID: 84894880303     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.0433     Document Type: Review

References (102)

1. Pittendrigh CS. 1982 Circadian organization and the photoperiodic phenomena. In Biological clocks in seasonal reproductive cycles (eds BK Follett, DE Follett), pp. 1-35. Bristol, UK: Wright.
2. Hut RA, Beersma DG. 2011 Evolution of timekeeping mechanisms: early emergence and adaptation to photoperiod. Phil. Trans. R. Soc. B 366, 2141-2154. (doi:10.1098/rstb.2010.0409)
3. Daan S, Aschoff J. 1975 Circadian rhythms of locomotor activity in captive birds and mammals: their variations with season and latitude. Oecologia 18, 269-316. (doi:10.1007/BF00345851)
4. Immelmann K. 1972 Erörterungen zur Definition und Anwendbarkeit der Begriffe 'ultimate factor', 'proximate factor', und 'zeitgeber'. Oecologia 9, 259-264. (doi:10.1007/BF00345235)
5. Bradshaw WE, Holzapfel CM. 2010 Light, time, and the physiology of biotic response to rapid climate change in animals. Annu. Rev. Physiol. 72, 147-166. (doi:10.1146/annurev-physiol-021909-135837)
6. Bradshaw WE. 1976 Geography of photoperiodic response in diapausing mosquito. Nature 262, 384-386. (doi:10.1038/262384b0)
7. International Civil Aviation Organization. 1993 Manual of the ICAO standard atmosphere (extended to 80 kilometres (262 500 feet), Doc 7488-CD, 3rd edn. Montréal, Canada: ICAO.
8. Tauber MJ, Tauber CA, Masaki S. 1986 Seasonal adaptations of insects. New York, NY: Oxford University Press.
9. Bale JS, Hayward SA. 2010 Insect overwintering in a changing climate. J. Exp. Biol. 213, 980-994. (doi:10.1242/jeb.037911)
10. Saunders DS. 1965 Larval diapause of maternal origin: induction of diapause in Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). J. Exp. Biol. 42, 495-508.
11. Danilevskii AS. 1965 Photoperiodism and seasonal development of insects. London, UK: Oliver & Boyd Ltd.
12. Danks HV. 1987 Insect dormancy: an ecological perspective. Ottawa, Canada: Biological Survey of Canada.
13. Wang XP, Yang QS, Dalin P, Zhou XM, Luo ZW, Lei CL. 2011 Geographic variation in photoperiodic diapause induction and diapause intensity in Sericinus montelus (Lepidoptera: Papilionidae). Insect Sci. 19, 295-302. (doi:10.1111/j.1744-7917.2011.01473. x)
14. Bradshaw WE, Quebodeaux MC, 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. (doi:10.1086/374344)
15. Kurota H, Shimada M. 2003 Geographical variation in photoperiodic induction of larval diapause in the bruchid beetle, Bruchidius dorsalis: polymorphism in overwintering stages. Entomol. Exp. Appl. 107, 11-18. (doi:10.1046/j.1570-7458.2003.00033. x)
16. Tauber MJ, Tauber CA. 1972 Geographic variation in critical photoperiod and in diapause intensity of Chrysopa carnea (Neuroptera). J. Insect Physiol. 18, 25-29. (doi:10.1016/0022-1910(72)90061-3)
17. Kikukawa S, Chippendale GM. 1984 Seasonal adaptations of different geographical populations of the sunflower moth, Homoeosoma electellum. J. Insect Physiol. 30, 451-455. (doi:10.1016/0022-1910(84)90024-6)
18. Suwa A, Gotoh T. 2006 Geographic variation in diapause induction and mode of diapause inheritance in Tetranychus pueraricola. J. Appl. Entomol. 130, 329-335. (doi:10.1111/j.1439-0418. 2006.01050. x)
19. Shimizu T, Kawasaki K. 2001 Geographic variability in diapause response of Japanese Orius species. Entomol. Exp. Appl. 98, 303-316. (doi:10.1046/j. 1570-7458.2001.00787. x)
20. Paolucci S, van de Zande L, Beukeboom LW. 2013 Adaptive latitudinal cline of photoperiodic diapause induction in the parasitoid Nasonia vitripennis in Europe. J. Evol. Biol. 26, 705-718. (doi:10.1111/jeb.12113)
21. Tyukmaeva VI, Salminen TS, Kankare M, Knott KE, Hoikkala A. 2011 Adaptation to a seasonally varying environment: a strong latitudinal cline in reproductive diapause combined with high gene flow in Drosophila montana. Ecol. Evol. 1, 160-168. (doi:10.1002/ece3.14)
22. Muona D, Lumme J. 1981 Geographical variation in the reproductive cycle and photoperiodic diapause of Drosophila phalerata and D. transversa (Drosophilidae: Diptera). Evolution 35, 158-167. (doi:10.2307/2407949)
23. Allemand R, David JR. 1976 The circadian rhythm of oviposition in Drosophila melanogaster: a genetic latitudinal cline in wild populations. Experientia 32, 1403-1405. (doi:10.1007/BF01937401)
24. Lankinen P. 1993 North-south differences in circadian eclosion rhythm in European populations of Drosophila subobscura. Heredity 71, 210-218. (doi:10.1038/hdy.1993.126)
25. Lankinen P. 1986 Geographical variation in circadian eclosion rhythm and photoperiodic adult diapause in Drosophila littoralis. J. Comp. Physiol. A 159, 123-142. (doi:10.1007/BF00612503)
26. Pittendrigh CS, Takamura T. 1989 Latitudinal clines in the properties of a circadian pacemaker. J. Biol. Rhythms 4, 217-235. (doi:10.1177/ 074873048900400209)
27. Bean DW, Dalin P, Dudley TL. 2012 Evolution of critical day length for diapause induction enables range expansion of Diorhabda carinulata, a biological control agent against tamarisk (Tamarix spp.). Evol. Appl. 5, 511-523. (doi:10.1111/j.1752-4571.2012.00262. x)
28. Gomi T. 2007 Seasonal adaptations of the fall webworm Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) following its invasion of Japan. Ecol. Res. 22, 855-861. (doi:10.1007/s11284-006-0327-y)
29. Sadakiyo S, Ishihara M. 2011 Rapid seasonal adaptation of an alien bruchid after introduction: geographic variation in life cycle synchronization and critical photoperiod for diapause induction. Entomol. Exp. Appl. 140, 69-76. (doi:10.1111/j. 1570-7458.2011.01136. x)
30. Bradshaw WE, Holzapfel CM. 2001 Genetic shift in photoperiodic response correlated with global warming. Proc. Natl Acad. Sci. USA 98, 14 509-14 511. (doi:10.1073/pnas.241391498)
31. Demont M, Blanckenhorn WU, Hosken DJ, Garner TW. 2008 Molecular and quantitative genetic differentiation across Europe in yellow dung flies. J. Evol. Biol. 21, 1492-1503. (doi:10.1111/j.1420-9101.2008.01615. x)
32. Leisnham PT, Towler L, Juliano SA. 2011 Geographic variation of photoperiodic diapause but not adult survival or reproduction of the invasive mosquito Aedes albopictus (Diptera: Culicidae) in North America. Ann. Entomol. Soc. Am. 104, 1309-1318. (doi:10.1603/AN11032)
33. Masaki S. 1999 Seasonal adaptations of insects as revealed by latitudinal diapause clines. Entomol. Sci. 2, 539-542.
34. Schmidt PS, Matzkin L, Ippolito M, Eanes WF. 2005 Geographic variation in diapause incidence, lifehistory traits, and climatic adaptation in Drosophila melanogaster. Evolution 59, 1721-1732. (doi:10. 1554/05-115.1)
35. Winterhalter WE, Mousseau TA. 2007 Patterns of phenotypic and genetic variation for the plasticity of diapause incidence. Evolution 61, 1520-1531. (doi:10.1111/j.1558-5646.2007.00127. x)
36. Miyazaki Y, Nisimura T, Numata H. 2005 A phase response curve for circannual rhythm in the varied carpet beetle Anthrenus verbasci. J. Comp. Physiol. A 191, 883-887. (doi:10.1007/s00359-005-0012-6)
37. Miyazaki Y, Nisimura T, Numata H. 2012 Circannual rhythm in the varied carpet beetle, Anthrenus verbasci. Prog. Brain Res. 199, 439-456. (doi:10. 1016/B978-0-444-59427-3.00025-3)
38. Beach R. 1978 The required day number and timely induction of diapause in geographic strains of mosquito Aedes atropalpus. J. Insect Physiol. 24, 449-455. (doi:10.1016/0022-1910(78)90088-4)
39. McWatters HG, Saunders DS. 1998 Maternal temperature has different effects on the photoperiodic response and duration of larval diapause in blow fly (Calliphora vicina) strains collected at two latitudes. Physiol. Entomol. 23, 369-375. (doi:10.1046/j.1365-3032.1998.00101. x)
40. Saunders DS. 1973 Thermoperiodic control of diapause in an insect: theory of internal coincidence. Science 181, 358-360. (doi:10.1126/ science.181.4097.358)
41. Saunders DS. 2002 Insect clocks, 3rd edn. Amsterdam, The Netherlands: Elsevier.
42. Goto SG. 2013 Roles of circadian clock genes in insect photoperiodism. Entomol. Sci. 16, 1-16. (doi:10.1111/ens.12000)
43. Mayer W. 1966 Besonderheiten der circadianen Rhythmik bei Pflanzen verschiedener geographischer Breiten. Planta 70, 237-256. (doi:10.1007/BF00396490)
44. Michael TP, Salome PA, Yu HJ, Spencer TR, Sharp EL, McPeek MA, Alonso JM, Ecker JR, McClung CR. 2003 Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302, 1049-1053. (doi:10.1126/science.1082971)
45. Pittendrigh CS, Kyner WT, Takamura T. 1991 The amplitude of circadian oscillations: temperature dependence, latitudinal clines, and the photoperiodic time measurement. J. Biol. Rhythms 6, 299-313. (doi:10.1177/074873049100600402)
46. Lankinen P, Forsman P. 2006 Independence of genetic geographical variation between photoperiodic diapause, circadian eclosion rhythm, and Thr-Gly repeat region of the period gene in Drosophila littoralis. J. Biol. Rhythms 21, 3-12. (doi:10.1177/0748730405283418)
47. Yammouni R, Bozzano A, Douglas RH. 2011 A latitudinal cline in the efficacy of endogenous signals: evidence derived from retinal cone contraction in fish. J. Exp. Biol. 214, 501-508. (doi:10.1242/jeb.048538)
48. Reimchen TE. 1987 Human color vision deficiencies and atmospheric twilight. Soc. Biol. 34, 1-11. (doi:10.1080/19485565.1987.9988655)
49. Verhulst S, Maes FW. 1998 Scotopic vision in colourblinds. Vis. Res. 38, 3387-3390. (doi:10.1016/ S0042-6989(97)00339-8)
50. Ciarleglio CM et al. 2008 Genetic differences in human circadian clock genes among worldwide populations. J. Biol. Rhythms 23, 330-340. (doi:10. 1177/0748730408320284)
51. Cruciani F, Trombetta B, Labuda D, Modiano D, Torroni A, Costa R, Scozzari R. 2008 Genetic diversity patterns at the human clock gene period 2 are suggestive of population-specific positive selection. Eur. J. Hum. Genet. 16, 1526-1534. (doi:10.1038/ejhg.2008.105)
52. Costa R, Peixoto AA, Barbujani G, Kyriacou CP. 1992 A latitudinal cline in a Drosophila clock gene. Proc. R. Soc. Lond. B 250, 43-49. (doi:10.1098/ rspb.1992.0128)
53. Sawyer LA, Sandrelli F, Pasetto C, Peixoto AA, Rosato E, Costa R, Kyriacou CP. 2006 The period gene Thr-Gly polymorphism in Australian and African Drosophila melanogaster populations: implications for selection. Genetics 174, 465-480. (doi:10.1534/genetics.106.058792)
54. Rosato E, Peixoto AA, Costa R, Kyriacou CP. 1997 Linkage disequilibrium, mutational analysis and natural selection in the repetitive region of the clock gene, period, in Drosophila melanogaster. Genet. Res. 69, 89-99. (doi:10.1017/S001667239700267X)
55. Sawyer LA, Hennessy JM, Peixoto AA, Rosato E, Parkinson H, Costa R, Kyriacou CP. 1997 Natural variation in a Drosophila clock gene and temperature compensation. Science 278, 2117-2120. (doi:10.1126/science.278.5346.2117)
56. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH. 1998 Resonating circadian clocks enhance fitness in cyanobacteria. Proc. Natl Acad. Sci. USA 95, 8660-8664. (doi:10.1073/pnas.95.15. 8660)
57. Suri V, Qian Z, Hall JC, Rosbash M. 1998 Evidence that the TIM light response is relevant to lightinduced phase shifts in Drosophila melanogaster. Neuron 21, 225-234. (doi:10.1016/S0896-6273(00)80529-2)
58. Yang Z, Emerson M, Su HS, Sehgal A. 1998 Response of the timeless protein to light correlates with behavioral entrainment and suggests a nonvisual pathway for circadian photoreception. Neuron 21, 215-223. (doi:10.1016/S0896-6273(00)80528-0)
59. Rosato E, Trevisan A, Sandrelli F, Zordan M, Kyriacou CP, Costa R. 1997 Conceptual translation of timeless reveals alternative initiating methionines in Drosophila. Nucleic Acids Res. 25, 455-458. (doi:10. 1093/nar/25.3.455)
60. Tauber E et al. 2007 Natural selection favors a newly derived timeless allele in Drosophila melanogaster. Science 316, 1895-1898. (doi:10. 1126/science.1138412)
61. Sandrelli F et al. 2007 A molecular basis for natural selection at the timeless locus in Drosophila melanogaster. Science 316, 1898-1900. (doi:10. 1126/science.1138426)
62. Bünning E. 1936 Die endogene Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber dtsch bot Ges 54, 590-607.
63. Sawa M, Nusinow DA, Kay SA, Imaizumi T. 2007 FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318, 261-265. (doi:10.1126/science.1146994)
64. Mathias D, Jacky L, Bradshaw WE, Holzapfel CM. 2007 Quantitative trait loci associated with photoperiodic response and stage of diapause in the pitcher-plant mosquito, Wyeomyia smithii. Genetics 176, 391-402. (doi:10.1534/genetics.106.068726)
65. Stehlik J, Zavodska R, Shimada K, Sauman I, Kostal V. 2008 Photoperiodic induction of diapause requires regulated transcription of timeless in the larval brain of Chymomyza costata. J. Biol. Rhythms 23, 129-139. (doi:10.1177/0748730407313364)
66. Yamada H, Yamamoto MT. 2011 Association between circadian clock genes and diapause incidence in Drosophila triauraria. PLoS ONE 6, e27493. (doi:10.1371/journal. pone.0027493)
67. Han B, Denlinger DL. 2009 Length variation in a specific region of the period gene correlates with differences in pupal diapause incidence in the flesh fly, Sarcophaga bullata. J. Insect Physiol. 55, 415-418. (doi:10.1016/j. jinsphys.2009.01.005)
68. Han B, Denlinger DL. 2009 Mendelian inheritance of pupal diapause in the flesh fly, Sarcophaga bullata. J. Hered. 100, 251-255. (doi:10.1093/jhered/ esn082)
69. Ikeno T, Numata H, Goto SG. 2011 Circadian clock genes period and cycle regulate photoperiodic diapause in the bean bug Riptortus pedestris males. J. Insect Physiol. 57, 935-938. (doi:10.1016/j. jinsphys.2011.04.006)
70. Ikeno T, Numata H, Goto SG. 2011 Photoperiodic response requires mammalian-type cryptochrome in the bean bug Riptortus pedestris. Biochem. Biophys. Res. Commun. 410, 394-397. (doi:10.1016/j. bbrc. 2011.05.142)
71. Ikeno T, Tanaka SI, Numata H, Goto SG. 2010 Photoperiodic diapause under the control of circadian clock genes in an insect. BMC Biol. 8, 116. (doi:10.1186/1741-7007-8-116)
72. Saunders DS, Bertossa RC. 2011 Deciphering time measurement: the role of circadian 'clock' genes and formal experimentation in insect photoperiodism. J. Insect Physiol. 57, 557-566. (doi:10.1016/j. jinsphys.2011.01.013)
73. Schiesari L, Kyriacou CP, Costa R. 2011 The hormonal and circadian basis for insect photoperiodic timing. FEBS Lett. 585, 1450-1460. (doi:10.1016/j. febslet.2011.02.026)
74. 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, 16 207-16 211. (doi:10.1073/ pnas.0805485105)
75. 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, 15 911-15 915. (doi:10.1073/pnas. 0604592103)
76. Paaby AB, Blacket MJ, Hoffmann AA, Schmidt PS. 2010 Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Mol. Ecol. 19, 760-774. (doi:10.1111/ j.1365-294X.2009.04508. x)
77. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, Garofalo RS. 2001 A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292, 107-110. (doi:10.1126/science.1057987)
78. Partridge L, Alic N, Bjedov I, Piper MD. 2011 Ageing in Drosophila: the role of the insulin/Igf and TOR signalling network. Exp. Gerontol. 46, 376-381. (doi:10.1016/j. exger.2010.09.003)
79. Sim C, Denlinger DL. 2008 Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc. Natl Acad. Sci. USA 105, 6777-6781. (doi:10.1073/pnas.0802067105)
80. Fidler AE, Gwinner E. 2003 Comparative analysis of avian BMAL1 and CLOCK protein sequences: a search for features associated with owl nocturnal behaviour. Comp. Biochem. Physiol. B 136, 861-874. (doi:10.1016/S1096-4959(03)00276-8)
81. Johnsen A et al. 2007 Avian clock gene polymorphism: evidence for a latitudinal cline in allele frequencies. Mol. Ecol. 16, 4867-4880. (doi:10.1111/j.1365-294X.2007.03552. x)
82. Dor R, Cooper CB, Lovette IJ, Massoni V, Bulit F, Liljesthrom M, Winkler DW. 2012 Clock gene variation in Tachycineta swallows. Ecol. Evol. 2, 95-105. (doi:10.1002/ece3.73)
83. Dor R et al. 2011 Low variation in the polymorphic clock gene poly-Q region despite population genetic structure across barn swallow (Hirundo rustica) populations. PLoS ONE 6, e28843. (doi:10.1371/ journal. pone.0028843)
84. O'Malley KG, Banks MA. 2008 A latitudinal cline in the Chinook salmon (Oncorhynchus tshawytscha) Clock gene: evidence for selection on PolyQ length variants. Proc. R. Soc. B 275, 2813-2821. (doi:10. 1098/rspb.2008.0524)
85. O'Malley KG, Ford MJ, Hard JJ. 2010 Clock polymorphism in Pacific salmon: evidence for variable selection along a latitudinal gradient. Proc. R. Soc. B 277, 3703-3714. (doi:10.1098/rspb. 2010.0762)
86. Dardente H, Wyse C, Birnie M, Dupré S, Loudon A, Lincoln G, Hazlerigg D. 2010 A molecular switch for photoperiod responsiveness in mammals. Curr. Biol. 20, 2193-2198. (doi:10.1016/j. cub.2010.10.048)
87. Krol E, Douglas A, Dardente H, Birnie MJ, Vinne V, Eijer WG, Gerkema MP, Hazlerigg DG, Hut RA. 2012 Strong pituitary and hypothalamic responses to photoperiod but not to 6-methoxy-2-benzoxazolinone in female common voles (Microtus arvalis). Gen. Comp. Endocrinol. 179, 289-295. (doi:10.1016/j. ygcen.2012.09.004)
88. Masumoto KH, Ukai-Tadenuma M, Kasukawa T, Nagano M, Uno KD, Tsujino K, Horikawa K, Shigeyoshi Y, Ueda HR. 2010 Acute induction of Eya3 by late-night light stimulation triggers TSHß expression in photoperiodism. Curr. Biol. 20, 2199-2206. (doi:10.1016/j. cub.2010.11.038)
89. Hut RA. 2011 Photoperiodism: shall EYA compare thee to a summer's day? Curr. Biol. 21, R22-R25. (doi:10.1016/j. cub.2010.11.060)
90. Pittendrigh CS. 1993 Temporal organisation: reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55, 17-54. (doi:10.1146/annurev. ph.55. 030193.000313)
91. Saunders DS. 1997 Insect circadian rhythms and photoperiodism. Invert Neurosci. 3, 155-164. (doi:10.1007/BF02480370)
92. Emerson KJ, Dake SJ, Bradshaw WE, Holzapfel CM. 2009 Evolution of photoperiodic time measurement is independent of the circadian clock in the pitcherplant mosquito, Wyeomyia smithii. J. Comp. Physiol. A 195, 385-391. (doi:10.1007/s00359-009-0416-9)
93. Comas M, Beersma DG, Spoelstra K, Daan S. 2006 Phase and period responses of the circadian system of mice (Mus musculus) to light stimuli of different duration. J. Biol. Rhythms 21, 362-372. (doi:10. 1177/0748730406292446)
94. Wever RA. 1967 Zum Einfluss der Dämmerung auf die circadiane Periodik. Ztschr f verg Physiol. 55, 255-277.
95. Boulos Z, Macchi M, Terman M. 1996 Effects of twilights on circadian entrainment patterns and reentrainment rates in squirrel monkeys. J. Comp. Physiol. A 179, 687-694. (doi:10.1007/ BF00216132)
96. Boulos Z, Macchi MM, Terman M. 2002 Twilights widen the range of photic entrainment in hamsters. J. Biol. Rhythms 17, 353-363. (doi:10.1177/ 074873002129002654)
97. Boulos Z, Macchi MM. 2005 Season-and latitudedependent effects of simulated twilights on circadian entrainment. J. Biol. Rhythms 20, 132-144. (doi:10.1177/0748730404272907)
98. Comas M, Hut RA. 2009 Twilight and photoperiod affect behavioral entrainment in the house mouse (Mus musculus). J. Biol. Rhythms 24, 403-412. (doi:10.1177/0748730409343873)
99. Baggs JE, Price TS, DiTacchio L, Panda S, FitzGerald GA, Hogenesch JB. 2009 Network features of the mammalian circadian clock. PLoS Biol. 7, e52. (doi:10.1371/journal. pbio.1000052)
100. O'Brien C, Bradshaw WE, Holzapfel CM. 2011 Testing for causality in covarying traits: genes and latitude in a molecular world. Mol. Ecol. 20, 2471-2476. (doi:10.1111/j.1365-294X.2011.05133. x)
101. Albrecht U, Zheng B, Larkin D, Sun ZS, Lee CC. 2001 mPer1 and mPer2 are essential for normal resetting of the circadian clock. J. Biol. Rhythms 16, 100-104. (doi:10.1177/074873001129001791)
102. Emerson KJ, Bradshaw WE, Holzapfel CM. 2009 Complications of complexity: integrating environmental, genetic and hormonal control of insect diapause. Trends Genet. 25, 217-225. (doi:10.1016/j. tig.2009.03.009)