Behavior Genetics

, Volume 43, Issue 3, pp 241–253 | Cite as

Circadian Rhythms and Period Expression in the Hawaiian Cricket Genus Laupala

Original Research

Abstract

Daily activity times and circadian rhythms of crickets have been a subject of behavioral and physiological study for decades. However, recent studies suggest that the underlying molecular mechanism of cricket endogenous clocks differ from the model of circadian rhythm generation in Drosophila. Here we examine the circadian free-running periods of walking and singing in two Hawaiian swordtail cricket species, Laupala cerasina and Laupala paranigra, that differ in the daily timing of mating related activities. Additionally, we examine variation in sequence and daily cycling of the period (per) gene transcript between these species. The species differed significantly in free-running period of singing, but did not differ significantly in the free-running period of locomotion. Like in Drosophila, per transcript abundance showed cycling consistent with a role in circadian rhythm generation. The amino acid differences identified between these species suggest a potential of the per gene in interspecific behavioral variation in Laupala.

Keywords

Laupala Cricket Courtship Circadian Period Free-running 

Notes

Acknowledgments

DJF was supported by an NIH training Grant (No. 5T32GM007469 to the Cornell graduate field of Neurobiology and Behavior). Parts of this work were supported by an NSF doctoral dissertation improvement grant (IOS0709993). We would like to thank Chris Wiley, Holly Menninger, Chris Ellison, and Biz Turnell for valuable discussion and feedback.

References

  1. Abdelsalam S, Uemura H, Umezaki Y, Saifullah ASM, Shimohigashi M, Tomioka K (2008) Characterization of PDF-immunoreactive neurons in the optic lobe and cerebral lobe of the cricket, Gryllus bimaculatus. J Insect Physiol 54(7):1205–1212PubMedCrossRefGoogle Scholar
  2. Abe Y, Ushirogawa H, Tomioka K (1997) Circadian locomotor rhythms in the cricket, Gyrllodes sigillatus. I. Localization of the pacemaker and the photoreceptor. Zool Sci 14(5):719–727PubMedCrossRefGoogle Scholar
  3. Alexander RD, Meral GH (1967) Seasonal and daily chirping cycles in the northern spring and fall field crickets, Gryllus veletis and G. pennsylvanicus. Ohio J Sci 67(4):200–209Google Scholar
  4. Bachleitner W, Kempinger L, Wulbeck C, Rieger D, Helfrich-Forster C (2007) Moonlight shifts the endogenous clock of Drosophila melanogaster. Proc Natl Acad Sci USA 104(9):3538–3543PubMedCrossRefGoogle Scholar
  5. Bae K, Edery I (2006) Regulating a circadian clock’s period, phase and amplitude by phosphorylation: insights from Drosophila. J Biochem 140(5):609–617PubMedCrossRefGoogle Scholar
  6. Bianchi DE (1964) Endogenous circadian rhythm in Neurospora crassa. J Gen Microbiol 35(3):437–445PubMedGoogle Scholar
  7. Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294(5):1351–1362PubMedCrossRefGoogle Scholar
  8. Chiba Y, Tomioka K (1987) Insect circadian activity with special reference to the localization of the pacemaker. Zool Sci 4(6):945–954Google Scholar
  9. Danbara Y, Sakamoto T, Uryu O, Tomioka K (2010) RNA interference of timeless gene does not disrupt circadian locomotor rhythms in the cricket Gryllus bimaculatus. J Insect Physiol 56(12):1738–1745PubMedCrossRefGoogle Scholar
  10. Danley PD, de Carvalho TN, Fergus DJ, Shaw KL (2007) Reproductive asynchrony and the divergence of Hawaiian crickets. Ethology 113(12):1125–1132CrossRefGoogle Scholar
  11. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96(2):271–290PubMedCrossRefGoogle Scholar
  12. Edery I, Zwiebel LJ, Dembinska ME, Rosbash M (1994) Temporal phosphorylation of the Drosophila period protein. Proc Natl Acad Sci USA 91(6):2260–2264PubMedCrossRefGoogle Scholar
  13. Engelmann W, Maurer A, Muhlbach M, Johnsson A (1974) Action of lithium ions and heavy-water in slowing circadian rhythms of petal movement in Kalanchoe. J Interdiscip Cycle Res 5(3–4):199–205CrossRefGoogle Scholar
  14. Ewer J, Frisch B, Hamblencoyle MJ, Rosbash M, Hall JC (1992) Expression of the period clock gene within different cell-types in the brain of Drosophila adults and mosaic analysis of these cells influence on circadian behavioral rhythms. J Neurosci 12(9):3321–3349PubMedGoogle Scholar
  15. Fergus DJ, de Carvalho TN, Shaw KL (2011) Genetic regulation of differential timing in courtship and mating of the Hawaiian cricket Laupala. Behav Genet 41(4):607–614PubMedCrossRefGoogle Scholar
  16. Gardner GF, Feldman JF (1980) The Frq locus in Neurospora crassa––a key element in circadian clock organization. Genetics 96(4):877–886PubMedGoogle Scholar
  17. Giebultowicz JM (2000) Molecular mechanism and cellular distribution of insect circadian clocks. Annu Rev Entomol 45:769–793PubMedCrossRefGoogle Scholar
  18. Guldemond JA, Tigges WT, Devrijer PWF (1994) Circadian-rhythm of sex-pheromone production and male activity of coexisting sibling species of Cryptomyzus aphids (Homoptera, Aphididae). Eur J Entomol 91(1):85–89Google Scholar
  19. Hamblen–Coyle MJ, Wheeler DA, Rutila JE, Rosbash M, Hall JC (1992) Behavior of period-altered circadian rhythm mutants of Drosophila in light-dark cycles (Diptera, Drosophilidae). J Insect Behav 5(4):417–446CrossRefGoogle Scholar
  20. Hardin PE (2005) The circadian timekeeping system of Drosophila. Curr Biol 15(17):R714–R722PubMedCrossRefGoogle Scholar
  21. Hassaneen E, Sallam AE, Abo-Ghalia A, Moriyama Y, Karpova SG, Abdelsalam S, Matsushima A, Shimohigashi Y, Tomioka K (2011) Pigment-dispersing factor affects nocturnal activity rhythms, photic entrainment, and the free-running period of the circadian clock in the cricket Gryllus bimaculatus. J Biol Rhythms 26(1):3–13PubMedCrossRefGoogle Scholar
  22. Helfrich-Forster C (2005) Organization of endogenous clocks in insects. Biochem Soc Trans 33:957–961PubMedCrossRefGoogle Scholar
  23. Helfrich-Forster C, Stengl M, Homberg U (1998) Organization of the circadian system in insects. Chronobiol Int 15(6):567–594PubMedCrossRefGoogle Scholar
  24. Huang TC, Lay KC, Tong SR (1991) Resetting the endogenous circadian N2-fixing rhythm of the prokaryote Synechococcus Rf-1. Bot Bul Acad Sin 32(2):129–133Google Scholar
  25. Kloss B, Rothenfluh A, Young MW, Saez L (2001) Phosphorylation of PERIOD is influenced by cycling physical associations of DOUBLE-TIME, PERIOD, and TIMELESS in the Drosophila clock. Neuron 30(3):699–706PubMedCrossRefGoogle Scholar
  26. Kondo T, Tsinoremas NF, Golden SS, Johnson CH, Kutsuna S, Ishiura M (1994) Circadian clock mutants of cyanobacteria. Science 266(5188):1233–1236PubMedCrossRefGoogle Scholar
  27. Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 68(9):2112–2116PubMedCrossRefGoogle Scholar
  28. Kyriacou CP, Hall JC (1980) Circadian-rhythm mutations in Drosophila melanogaster affect short-term fluctuations in the male’s courtship song. Proc Natl Acad Sci USA 77(11):6729–6733PubMedCrossRefGoogle Scholar
  29. Lecharny A, Wagner E (1984) Stem extension rate in light grown plants-evidence for an endogenous circadian rhythm in Chenopodium rubrum. Physiol Plant 60(3):437–443CrossRefGoogle Scholar
  30. Lee CG, Bae KH, Edery I (1998) The Drosophila CLOCK protein undergoes daily rhythms in abundance, phosphorylation, and interactions with the PER–TIM complex. Neuron 21(4):857–867PubMedCrossRefGoogle Scholar
  31. Lin GGH, Liou RF, Lee HJ (2002) The period gene of the German cockroach and its novel linking power between vertebrate and invertebrate. Chronobiol Int 19(6):1023–1040PubMedCrossRefGoogle Scholar
  32. Liu C, Li SM, Liu TH, Borjigin J, Lin JD (2007) Transcriptional coactivator PGC––1a integrates the mammalian clock and energy metabolism. Nature 447(7143):477–481PubMedCrossRefGoogle Scholar
  33. Loher W (1972) Circadian control of stridulation in the cricket Teleogryllus commodus walker. J Comp Physiol 79(2):173–190CrossRefGoogle Scholar
  34. Loher W (1974) Circadian control of spermatophore formation in the cricket Teleogryllus commodus walker. J Insect Physiol 20(7):1155–1172PubMedCrossRefGoogle Scholar
  35. Lupien M (1998) Correlation between ultradian and circadian rhythms in the cricket, Teleogryllus oceanicus: potential role for the period gene. Department of Biology, McGill University, Montreal, p 66Google Scholar
  36. Lupien M, Marshall S, Leser W, Pollack GS, Honegger HW (2003) Antibodies against the PER protein of Drosophila label neurons in the optic lobe, central brain, and thoracic ganglia of the crickets Teleogryllus commodus and Teleogryllus oceanicus. Cell Tissue Res 312(3):377–391PubMedCrossRefGoogle Scholar
  37. Mazor M, Dunkelblum E (2005) Circadian rhythms of sexual behavior and pheromone titers of two closely related moth species Autographa gamma and Cornutiplusia circumflexa. J Chem Ecol 31(9):2153–2168PubMedCrossRefGoogle Scholar
  38. Mazzoni CJ, Gomes CA, Souza NA, de Queiroz RG, Justiniano SCB, Ward RD, Kyriacou CP, Peixoto AA (2002) Molecular evolution of the period gene in sandflies. J Mol Evol 55(5):553–562PubMedCrossRefGoogle Scholar
  39. McFarlane JE (1968) Diel periodicity in spermatophore formation in house cricket Acheta domesticus (L). Can J Zool 46(4):695–698CrossRefGoogle Scholar
  40. Millar AJ, Kay SA (1991) Circadian control of cab gene-transcription and messenger-RNA accumulation in Arabidopsis. Plant Cell 3(5):541–550PubMedGoogle Scholar
  41. Miyatake T (2002) Pleiotropic effect, clock genes, and reproductive isolation. Popul Ecol 44(3):201–207CrossRefGoogle Scholar
  42. Miyatake T, Kanmiya K (2004) Male courtship song in circadian rhythm mutants of Bactrocera cucurbitae (Tephritidae:Diptera). J Insect Physiol 50(1):85–91PubMedCrossRefGoogle Scholar
  43. Miyatake T, Matsumoto A, Matsuyama T, Ueda HR, Toyosato T, Tanimura T (2002) The period gene and allochronic reproductive isolation in Bactrocera cucurbitae. Proc R Soc Lond B Biol Sci 269(1508):2467–2472CrossRefGoogle Scholar
  44. Moriyama Y, Sakamoto T, Karpova SG, Matsumoto A, Noji S, Tomioka K (2008) RNA interference of the clock gene period disrupts circadian rhythms in the cricket Gryllus bimaculatus. J Biol Rhythms 23(4):308–318PubMedCrossRefGoogle Scholar
  45. Moriyama Y, Sakamoto T, Matsumoto A, Noji S, Tomioka K (2009) Functional analysis of the circadian clock gene period by RNA interference in nymphal crickets Gryllus bimaculatus. J Insect Physiol 55(5):396–400PubMedCrossRefGoogle Scholar
  46. Myers MP, Wager–Smith K, Rothenfluh–Hilfiker A, Young MW (1996) Light-induced degradation of TIMELESS and entrainment of the Drosophila circadian clock. Science 271(5256):1736–1740PubMedCrossRefGoogle Scholar
  47. Nowosielski JW, Patton RL (1963) Studies on circadian rhythm of the house cricket Gryllus domesticus L. J Insect Physiol 9(4):401–404CrossRefGoogle Scholar
  48. Nowosielski JW, Patton RL (1964) Daily fluctuation in blood sugar concentration of house cricket Gryllus domesticus L. Science 144(361):180–181PubMedCrossRefGoogle Scholar
  49. Oh KP, Fergus DJ, Grace JL, Shaw KL (2012) Interspecific genetics of speciation phenotypes: song and preference coevolution in Hawaiian crickets. J Evol Biol 25(8):1500–1512PubMedCrossRefGoogle Scholar
  50. Otte D (1994) The Crickets of Hawaii. The Orthopterist’s Society, PhiladelphiaGoogle Scholar
  51. Petersen G, Hall JC, Rosbash M (1988) The period gene of Drosophila carries species-specific behavioral instructions. EMBO J 7(12):3939–3947PubMedGoogle Scholar
  52. Refinetti R (1996) Ultradian rhythms of body temperature and locomotor activity in wild-type and tau-mutant hamsters. Anim Biol 5(3):111–115Google Scholar
  53. Rieger D, Shafer OT, Tomioka K, Helfrich–Forster C (2006) Functional analysis of circadian pacemaker neurons in Drosophila melanogaster. J Neurosci 26(9):2531–2543PubMedCrossRefGoogle Scholar
  54. Rosato E, Tauber E, Kyriacou CP (2006) Molecular genetics of the fruit-fly circadian clock. Eur J Hum Genet 14(6):729–738PubMedCrossRefGoogle Scholar
  55. Ruf T (1999) The Lomb–Scargle periodogram in biological rhythm research: analysis of incomplete and unequally spaced time-series. Biol Rhythm Res 30(2):178–201CrossRefGoogle Scholar
  56. Sandrelli F, Tauber E, Pegoraro M, Mazzotta G, Cisotto P, Landskron J, Stanewsky R, Piccin A, Rosato E, Zordan M, Costa R, Kyriacou CP (2007) A molecular basis for natural selection at the timeless locus in Drosophila melanogaster. Science 316(5833):1898–1900PubMedCrossRefGoogle Scholar
  57. Sandrelli F, Costa R, Kyriacou CP, Rosato E (2008) Comparative analysis of circadian clock genes in insects. Insect Mol Biol 17(5):447–463PubMedCrossRefGoogle Scholar
  58. Shafer OT, Rosbash M, Truman JW (2002) Sequential nuclear accumulation of the clock proteins period and timeless in the pacemaker neurons of Drosophila melanogaster. J Neurosci 22(14):5946–5954PubMedGoogle Scholar
  59. Shao QM, Sehadova H, Ichihara N, Sehnal F, Takeda M (2006) Immunoreactivities to three circadian clock proteins in two ground crickets suggest interspecific diversity of the circadian clock structure. J Biol Rhythms 21(2):118–131PubMedCrossRefGoogle Scholar
  60. Shao QM, Bembenek J, Trang LTD, Hiragaki S, Takeda M (2008a) Molecular structure, expression patterns, and localization of the circadian transcription modulator CYCLE in the cricket Dianemobius nigrofasciatus. J Insect Physiol 54(2):403–413PubMedCrossRefGoogle Scholar
  61. Shao QM, Hiragaki S, Takeda M (2008b) Co-localization and unique distributions of two clock proteins CYCLE and CLOCK in the cephalic ganglia of the ground cricket, Allonemobius allardi. Cell Tissue Res 331(2):435–446PubMedCrossRefGoogle Scholar
  62. Shaw KL (1996) Polygenic inheritance of a behavioral phenotype:interspecific genetics of song in the Hawaiian cricket genus Laupala. Evolution 50(1):256–266CrossRefGoogle Scholar
  63. Shaw KL (2000a) Further acoustic diversity in Hawaiian forests: two new species of Hawaiian cricket (Orthoptera : Gryllidae : Trigonidiinae : Laupala). Zool J Linn Soc-Lond 129(1):73–91CrossRefGoogle Scholar
  64. Shaw KL (2000b) Interspecific genetics of mate recognition: inheritance of female acoustic preference in Hawaiian crickets. Evolution 54(4):1303–1312PubMedGoogle Scholar
  65. Shiga S, Numata H, Yoshioka E (1999) Localization of the photoreceptor and pacemaker for the circadian activity rhythm in the band-legged ground cricket, Dianemobius nigrofasciatus. Zool Sci 16(2):193–201CrossRefGoogle Scholar
  66. Shimizu T, Miyatake T, Watari Y, Arai T (1997) A gene pleiotropically controlling developmental and circadian periods in the melon fly, Bactrocera cucurbitae (Diptera:Tephritidae). Heredity 79:600–605CrossRefGoogle Scholar
  67. Shirasu N, Shimohigashi Y, Tominaga Y, Shimohigashi M (2003) Molecular cogs of the insect circadian clock. Zool Sci 20(8):947–955PubMedCrossRefGoogle Scholar
  68. Sokolove PG (1975) Locomotory and stridulatory circadian rhythms in the cricket, Teleogryllus commodus. J Insect Physiol 21(3):537–558PubMedCrossRefGoogle Scholar
  69. Sokolove PG, Loher W (1975) Role of eyes, optic lobes, and pars intercerebralis in locomotory and stridulatory circadian rhythms of Teleogryllus commodus. J Insect Physiol 21(4):785–799PubMedCrossRefGoogle Scholar
  70. Tauber E, Roe H, Costa R, Hennessy JM, Kyriacou CP (2003) Temporal mating isolation driven by a behavioral gene in Drosophila. Curr Biol 13(2):140–145PubMedCrossRefGoogle Scholar
  71. 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(5833):1895–1898PubMedCrossRefGoogle Scholar
  72. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W:improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680PubMedCrossRefGoogle Scholar
  73. Tomioka K, Abdelsalam S (2004) Circadian organization in hemimetabolous insects. Zool Sci 21(12):1153–1162PubMedCrossRefGoogle Scholar
  74. Tomioka K, Chiba Y (1992) Characterization of an optic lobe circadian pacemaker by in situ and in vitro recording of neural activity in the cricket, Gryllus bimaculatus. J Comp Physiol A 171(1):1–7CrossRefGoogle Scholar
  75. Weber F (2009) Remodeling the clock:coactivators and signal transduction in the circadian clockworks. Naturwissenschaften 96(3):321–337PubMedCrossRefGoogle Scholar
  76. Wheeler D, Kyriacou C, Greenacre M, Yu Q, Rutila J, Rosbash M, Hall J (1991) Molecular transfer of a species-specific behavior from Drosophila simulans to Drosophila melanogaster. Science 251(4997):1082–1085PubMedCrossRefGoogle Scholar
  77. Wiedenmann G, Loher W (1984) Circadian control of singing in crickets––2 different pacemakers for early-evening and before-dawn activity. J Insect Physiol 30(2):145–151CrossRefGoogle Scholar
  78. Yerushalmi S, Green RM (2009) Evidence for the adaptive significance of circadian rhythms. Ecol Lett 12(9):970–981PubMedCrossRefGoogle Scholar
  79. Yu W, Hardin PE (2006) Circadian oscillators of Drosophila and mammals. J Cell Sci 119(23):4793–4795PubMedCrossRefGoogle Scholar
  80. Zheng XZ, Sehgal A (2008) Probing the relative importance of molecular oscillations in the circadian clock. Genetics 178(3):1147–1155PubMedCrossRefGoogle Scholar
  81. Zheng B, Larkin DW, Albrecht U, Zhong Sheng S, Sage M, Eichele G, Cheng Chi L, Bradley A (1999) The mPer2 gene encodes a functional component of the mammalian circadian clock. Nature 400(6740):169–173PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Neurobiology and BehaviorCornell UniversityIthacaUSA

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