Many physiological processes of living organisms show circadian rhythms, governed by an endogenous clock. This clock has a genetic basis and is entrained by external cues, such as light and temperature. Other physiological processes exhibit seasonal rhythms, that are also responsive to light and temperature. We previously reported a natural latitudinal cline of photoperiodic diapause induction in the parasitic wasp Nasonia vitripennis in Europe and a correlated haplotype frequency for the circadian clock gene period (per). To evaluate if this correlation is reflected in circadian behaviour, we investigated the circadian locomotor activity of seven populations from the cline. We found that the proportion of rhythmic males was higher than females in constant darkness, and that mating decreased rhythmicity of both sexes. Only for virgin females, the free running period (τ) increased weakly with latitude. Wasps from the most southern locality had an overall shorter free running rhythm and earlier onset, peak, and offset of activity during the 24 h period, than wasps from the northernmost locality. We evaluated this variation in rhythmicity as a function of period haplotype frequencies in the populations and discussed its functional significance in the context of local adaptation.

Groningen Institute for Evolutionary Life Sciences University of Groningen 9712 CP Groningen The Netherlands

Institute of Entomology Biology Center of the Czech Academy of Sciences 370 05 Ceske Budejovice Czech Republic

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Pittendrigh C.S., Kyner W.T., Takamura T. The Amplitude of circadian oscillations: Temperature dependence, latitudinal clines, and the photoperiodic time measurement. J. Biol. Rhythm. 1991;6:299–313. doi: 10.1177/074873049100600402. PubMed DOI

Bradshaw W.E., Holzapfel C.M. Evolution of animal photoperiodism. Annu. Rev. Ecol. Evol. Syst. 2007;38:1–25. doi: 10.1146/annurev.ecolsys.37.091305.110115. DOI

Bunning E. Circadian rhythms and the mime measurement in photoperiodism. Cold Spring Harb. Symp. Quant. Biol. 1960;25:249–256. doi: 10.1101/SQB.1960.025.01.026. PubMed DOI

Saunders D.S. Controversial aspects of photoperiodism in insects and mites. J. Insect Physiol. 2010;56:1491–1502. doi: 10.1016/j.jinsphys.2010.05.002. PubMed DOI

Koštál V. Insect photoperiodic calendar and circadian clock: Independence, cooperation, or unity? J. Insect Physiol. 2011;57:538–556. doi: 10.1016/j.jinsphys.2010.10.006. PubMed DOI

Mukai A., Goto S.G. The clock gene period is essential for the photoperiodic response in the jewel wasp Nasonia vitripennis (Hymenoptera: Pteromalidae) Appl. Entomol. Zool. 2016;51:185–194. doi: 10.1007/s13355-015-0384-1. DOI

Urbanová V., Bazalová O., Vaněčková H., Dolezel D. Photoperiod regulates growth of male accessory glands through juvenile hormone signaling in the linden bug, Pyrrhocoris apterus. Insect Biochem. Mol. Biol. 2016;70:184–190. doi: 10.1016/j.ibmb.2016.01.003. PubMed DOI

Dalla Benetta E., Beukeboom L.W., van de Zande L. Adaptive differences in circadian clock gene expression patterns and photoperiodic diapause induction in Nasonia vitripennis. Am. Nat. 2019;193:881–896. doi: 10.1086/703159. PubMed DOI

Hut R.A., Paolucci S., Dor R., Kyriacou C.P., Daan S. Latitudinal clines: An evolutionary view on biological rhythms. Proc. R. Soc. B. 2013;280:20130433. doi: 10.1098/rspb.2013.0433. PubMed DOI PMC

Hut R.A., Beersma D.G.M. Evolution of time-keeping mechanisms: Early emergence and adaptation to photoperiod. Philos. Trans. R. Soc. B Biol. Sci. 2011;366:2141–2154. doi: 10.1098/rstb.2010.0409. PubMed DOI PMC

Paolucci S., van de Zande L., Beukeboom L.W. Adaptive latitudinal cline of photoperiodic diapause induction in the parasitoid Nasonia vitripennis in Europe. J. Evol. Biol. 2013;26:705–718. doi: 10.1111/jeb.12113. PubMed DOI

Saunders D.S. Insect photoperiodism: measuring the night. J. Insect Physiol. 2013;59:1–10. doi: 10.1016/j.jinsphys.2012.11.003. PubMed DOI

Saunders D.S. Photoperiodism and time measurement in the parasitic wasp, Nasonia vitripennis. J. Insect Physiol. 1968;14:433–450. doi: 10.1016/0022-1910(68)90060-7. DOI

Paolucci S., Salis L., Vermeulen C.J., Beukeboom L.W., van de Zande L. QTL analysis of the photoperiodic response and clinal distribution of period alleles in Nasonia vitripennis. Mol. Ecol. 2016;25:4805–4817. doi: 10.1111/mec.13802. PubMed DOI

Schmid B., Helfrich-Förster C., Yoshii T. A new ImageJ plug-in “ActogramJ” for chronobiological analyses. J. Biol. Rhythm. 2011;26:464–467. doi: 10.1177/0748730411414264. PubMed DOI

Sokolove P.G., Bushell W.N. The chi square periodogram: Its utility for analysis of circadian rhythms. J. Theor. Biol. 1978;72:131–160. doi: 10.1016/0022-5193(78)90022-X. PubMed DOI

Schlichting M., Helfrich-Förster C. Photic entrainment in Drosophila assessed by locomotor activity recordings. Methods Enzymol. 2015;552:105–123. PubMed

Floessner T.S.E., Boekelman F.E., Druiven S.J.M., de Jong M., Rigter P.M.F., Beersma D.G.M., Hut R.A. Lifespan is unaffected by size and direction of daily phase shifts in Nasonia, a hymenopteran insect with strong circadian light resetting. J. Insect Physiol. 2019;117:103896. doi: 10.1016/j.jinsphys.2019.103896. PubMed DOI

Bertossa R.C., van Dijk J., Diao W., Saunders D., Beukeboom L.W., Beersma D.G.M. Circadian rhythms differ between sexes and closely related species of Nasonia wasps. PLoS ONE. 2013;8:e60167. doi: 10.1371/journal.pone.0060167. PubMed DOI PMC

Sharma V., Lone S., Goel A., Chandrashekaran M.K. Circadian consequences of social organization in the ant species Camponotus compressus. Naturwissenschaften. 2004;91:386–390. doi: 10.1007/s00114-004-0544-6. PubMed DOI

Kauranen H., Menegazzi P., Costa R., Helfrich-Förster C., Kankainen A., Hoikkala A. Flies in the north: Locomotor behavior and clock neuron organization of Drosophila montana. J. Biol. Rhythm. 2012;27:377–387. doi: 10.1177/0748730412455916. PubMed DOI

Prabhakaran P.M., Sheeba V. Sympatric Drosophilid species melanogaster and ananassae differ in temporal patterns of activity. J. Biol. Rhythm. 2012;27:365–376. doi: 10.1177/0748730412458661. PubMed DOI

Prabhakaran P.M., Sheeba V. Insights into differential activity patterns of drosophilids under semi-natural conditions. J. Exp. Biol. 2013;216:4691–4702. doi: 10.1242/jeb.092270. PubMed DOI

Michael T.P. Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science. 2003;302:1049–1053. doi: 10.1126/science.1082971. PubMed DOI

Shinkawa Y., Takeda S., Tomioka K., Matsumoto A., Oda T., Chiba Y. Variability in circadian activity patterns within the Culex pipiens complex (Diptera: Culicidae) J. Med. Entomol. 1994;31:49–56. doi: 10.1093/jmedent/31.1.49. PubMed DOI

Pivarciova L., Vaneckova H., Provaznik J., Wu B.C.-H., Pivarci M., Peckova O., Bazalova O., Cada S., Kment P., Kotwica-Rolinska J., et al. Unexpected geographic variability of the free running period in the linden bug Pyrrhocoris apterus. J. Biol. Rhythm. 2016;31:568–576. doi: 10.1177/0748730416671213. PubMed DOI

Helfrich-Förster C., Bertolini E., Menegazzi P. Flies as models for circadian clock adaptation to environmental challenges. Eur. J. Neurosci. 2018 doi: 10.1111/ejn.14180. PubMed DOI PMC

Majercak J., Chen W.F., Edery I. Splicing of the period gene 3′-terminal intron is regulated by light, circadian clock factors, and phospholipase C. Mol. Cell Biol. 2004;24:3359–3372. doi: 10.1128/MCB.24.8.3359-3372.2004. PubMed DOI PMC

Low K.H., Lim C., Ko H.W., Edery I. Natural variation in the splice site strength of a clock gene and species-specific thermal adaptation. Neuron. 2008;60:1054–1067. doi: 10.1016/j.neuron.2008.10.048. PubMed DOI PMC