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Locomotor activity patterns in three spider species suggest relaxed selection on endogenous circadian period and novel features of chronotype

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Abstract

We examined the circadian rhythms of locomotor activity in three spider species in the Family Theridiidae under light–dark cycles and constant darkness. Contrary to previous findings in other organisms, we found exceptionally high variability in endogenous circadian period both within and among species. Many individuals exhibited circadian periods much lower (19–22 h) or much higher (26–30 h) than the archetypal circadian period. These results suggest relaxed selection on circadian period as well as an ability to succeed in nature despite a lack of circadian resonance with the 24-h daily cycle. Although displaying similar entrainment waveforms under light–dark cycles, there were remarkable differences among the three species with respect to levels of apparent masking and dispersion of activity under constant dark conditions. These behavioral differences suggest an aspect of chronotype adapted to the particular ecologies of the different species.

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References

  • Abraham U, Granada AE, Westermark PO, Heine M, Kramer A, Herzel H (2010) Coupling governs entrainment range of circadian clocks. Mole Syst Biol 6:438. https://doi.org/10.1038/msb.2010.92

    Article  Google Scholar 

  • Allada R, Emery P, Takahashi JS, Rosbash M (2001) Stopping time: the genetics of fly and mouse circadian clocks. Ann Rev Neurosci 24:1091–1119

    CAS  PubMed  Google Scholar 

  • Allebrandt KV, Roenneberg T (2008) The search for circadian clock components in humans: new perspectives for association studies. Braz J Med Res 41:716–721

    CAS  Google Scholar 

  • Ames A (2000) CNS energy metabolism as related to function. Brain Res Re 34:42–68

    CAS  Google Scholar 

  • Aschoff J (1979) Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. Z Tierpsychol 49:225–249

    CAS  PubMed  Google Scholar 

  • Barrett RK, Page TL (1989) effects of light on circadian pacemaker development. I. The freerunning period. J Comp Physiol 165:41–49

    CAS  Google Scholar 

  • Bartell PA, Gwinner E (2005) A separate circadian oscillator controls nocturnal migratory restlessness in the songbird Sylvia borin. J Biol Rhythms 20:538–549

    PubMed  Google Scholar 

  • Beaver LM, Gvakharia BO, Vollintine TS, Hege DM, Stanewsky R, Giebultowicz JM (2002) Loss of circadian clock function decreases reproductive fitness in males of Drosophila melanogaster. Proc Nat Acad Sci USA 99:2134–2139

    CAS  PubMed  Google Scholar 

  • Beaver LM, Rush BL, Gvakharia BO, Giebultowicz JM (2003) Noncircadian regulation and function of clock genes period and timeless in oogenesis of Drosophila melanogaster. J Biol Rhythms 18:463–472

    CAS  PubMed  Google Scholar 

  • Bertossa RC, van Dijk J, Diao W, Saunders D, Beukeboom LW, Beersma DGM (2013) Circadian rhythms differ between sexes and closely related species of Nasonia wasps. PLoS ONE 8(3):e60167. https://doi.org/10.1371/journal.pone.0060167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloch G, Robinson GE (2001) Reversal of honeybee behavioural rhythms. Nature 410:1048

    CAS  PubMed  Google Scholar 

  • Bloch G, Toma DP, Robinson GE (2001) Behavioral rhythmicity, age, division of labor and period expression in the honeybee brain. J Biol Rhythms 16:444–456

    CAS  PubMed  Google Scholar 

  • Brach V (1977) Anelosimus studiosus (Araneae: Theridiidae) and the evolution of quasisociality in theridiid spiders. Evolution 31:154–161

    PubMed  Google Scholar 

  • Bradley RA (2013) Common spiders of North America. University of California Press, Los Angeles

    Google Scholar 

  • Brown SA, Kunz D, Dumas A, Westermark PO, Vanselow K, Tilmann-Wahnschaffe A, Herzel H, Kramer A (2008) Molecular insights into human daily behavior. Proc Nat Acad Sci USA 105:1602–1607

    CAS  PubMed  Google Scholar 

  • Christensen ND, Lewis R (1982) the circadian locomotor rhythms of Hemideina thoracica (Orthoptera, Stenopelmatidae): the circadian clock as a population of interacting oscillators. Physiol Entomol 7:1–13

    Google Scholar 

  • Czeisler CA, Duffy JF, Shanahan TL, Brown EN, Mitchell JF, Rimmer DW, Ronda JM, Silva EJ, Allan JS, Emens JS, Dijk DJ, Kronauer RE (1999) Stability, precision, and near-24-hour period of the human circadian pacemaker. Science 284:2177–2181

    CAS  PubMed  Google Scholar 

  • Daan S, Berde C (1978) Two coupled oscillators: simulations of the circadian pacemaker in mammalian activity rhythms. J Theoret Biol 70:297–313

    CAS  Google Scholar 

  • Daan S, Beersma DGM (2002) Circadian frequency and its variability. In: Kumar V (ed) Biological rhythms. Springer, Berlin, pp 24–37

    Google Scholar 

  • DeCoursey PJ (1990) Circadian photoentrainment in nocturnal mammals: ecological overtones. Biol Behav 15:213–238

    Google Scholar 

  • DeCoursey PJ (2004) The behavioral ecology and evolution of biological timing systems. In: Dunlap JC, Loros JJ, DeCoursey PJ (eds) Chronobiology: biological timekeeping. Sunderland, MA, Sinauer, pp 27–65

    Google Scholar 

  • DeCoursey PJ, Walker JK, Smith SA (2000) A circadian pacemaker in free-living chipmunks: essential for survival? J Comp Physiol A 186:169–180

    CAS  PubMed  Google Scholar 

  • Dodd AN, Salathia N, Hall A, Keyei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633

    CAS  PubMed  Google Scholar 

  • Dominoni DM, Helm B, Lehmann M, Dowse HB, Partecke J (2013) Clocks for the city: circadian differences between forest and city songbirds. Proc Roy Soc B 280:20130593

    CAS  Google Scholar 

  • Dubowy C, Sehgal A (2017) Circadian rhythms and sleep in Drosophila melanogaster. Genetics 205:1373–1397

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duffy JF, Rimmer DW, Czeisler CA (2001) Association of intrinsic circadian period with morningness-eveningness, usual wake time, and circadian phase. Behav Neurosci 115:895–899

    CAS  PubMed  Google Scholar 

  • Dunlap JC (1996) Genetic and molecular analysis of circadian rhythms. Annu Rev Genet 30:579–601

    CAS  PubMed  Google Scholar 

  • Ebihara S, Tsuji K, Kondo K (1978) Strain differences of the mouse’s free-running circadian rhythm in continuous darkness. Physiol Behav 20:795–799

    CAS  PubMed  Google Scholar 

  • Emerson KJ, Bradshaw WE, Holzapfel CM (2009) Concordance of the circadian clock with the environment is necessary to maximize fitness in natural populations. Evolution 62–4:979–983

    Google Scholar 

  • Ewing HE (1918) The life and behavior of the house spider. Proc Iowa Acad Sci 25:177–204

    Google Scholar 

  • Fleury F, Allemand R, Vavre F, Fouillet P, Bouletreau M (2000) Adaptive significance of a circadian clock: temporal segregation of activities reduces intrinsic competitive inferiority in Drosophila parasitoids. Proc R Soc Lond B 267:1005–1010

    CAS  Google Scholar 

  • Fonken LK, Workman JL, Walton JC, Weil ZM, Morris JS, Haim A, Nelson RJ (2010) Light at night increases body mass by shifting the time of food intake. Proc Nat Acad Sci USA 107:18664–18669

    CAS  PubMed  Google Scholar 

  • Fonken LK, Aubrecht TG, Melendez-Fernandez H, Weil ZM, Nelson RJ (2013) Dim light at night disrupts molecular circadian rhythms and affects metabolism. J Biol Rhythms 28:262–271

    PubMed  PubMed Central  Google Scholar 

  • Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233

    Google Scholar 

  • Garmany M, Moore D, Jones TC (2019) Diel and circadian rhythms of locomotor activity in male Parasteatoda tepidariorum (Araneae: Theridiidae). J Arachnol 47:310–316

    Google Scholar 

  • Gerkema MP, Groos GA, Daan S (1990) Differential elimination of circadian and ultradian rhythmicity by hypothalamic lesions in the common vole Microtus arvalis. J Biol Rhythms 5:81–95

    CAS  PubMed  Google Scholar 

  • Gerkema MP, van der Leest F (1991) Ongoing ultradian activity rhythms in the common vole, Microtus arvalis, during deprivations of food, water and rest. J Comp Physiol A 168:591–597

    CAS  PubMed  Google Scholar 

  • Halberg F, Cornélissen G, Katinas G, Syutkina EV, Sothern RB, Zaslavskaya R, Halberg F, Watanabe Y, Schwartzkopff O, Otsuka K, Tarquini R, Frederico P, Siggelova J (1950s) Transdisciplinary unifying implications of circadian findings in the 1950s. J Circadian Rhythms 1:2

    PubMed  PubMed Central  Google Scholar 

  • Hall JC (1995) Tripping along the trail to the molecular mechanisms of biological clocks. Trends Neurosci 18:230–240

    CAS  PubMed  Google Scholar 

  • Hamblen MJ, White NE, Emery PTJ, Kaiser K, Hall JC (1998) Molecular and behavioral analysis of four period mutants in Drosophila melanogaster encompassing extreme short, novel long, and unorthodox arrhythmic types. Genetics 149:165–178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hassaneen E, Sallam AE, Abo-Ghalia A, Moriyama Y, Karpova SG, Abdelsalam S, Matushima 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 26:3–13

    CAS  PubMed  Google Scholar 

  • Helm B, Visser ME (2010) Heritable circadian period length in a wild bird population. Proc R Soc B 277:3335–3342

    PubMed  Google Scholar 

  • Helm B, Visser ME, Schwartz W, Kronfeld-Schor N, Gerkema M, Piersma T, Bloch G (2017) Two sides of a coin: ecological and chronobiological perspectives of timing in the wild. Phil Trans R Soc B 372:20160246. https://doi.org/10.1098/rstb.2016.0246

    Article  PubMed  Google Scholar 

  • Hódar JA, Sánchez-Piñero F (2002) Feeding habits of the black widow spider Latrodectus lilianae (Araneae: Theridiidae) in an arid zone of south-east Spain. J Zool 257:101–109

    Google Scholar 

  • Johnson CH (1992) Phase response curves: What can they tell us about circadian clocks? In: Hiroshige T, Honma K (eds) Circadian clocks from cell to human. Hokkaido University Press, Sapporo, pp 209–246

    Google Scholar 

  • Johnson CH, Elliott JA, Foster R (2003) Entrainment of circadian programs. Chronobiol Int 20:741–774

    PubMed  Google Scholar 

  • Johnson CH, Elliott J, Foster R, Honma K-I, Kronauer R (2004) Fundamental properties of circadian rhythms. In: Dunlap JC, Loros JJ, DeCoursey PJ (eds) Chronobiology: biological timekeeping. Sunderland, MA, Sinauer, pp 67–105

    Google Scholar 

  • Jones TC, Parker PG (2002) Delayed dispersal benefits both mother and offspring in the cooperative spider Anelosimus studiosus (Araneae: Theridiidae). Behav Ecol 13:142–148

    Google Scholar 

  • Jones TC, Wilson R, Moore D (2018) Circadian rhythms of locomotor activity in Metazygia wittfeldae (Araneae: Araneidae). J Arachnology 46:26–30

    Google Scholar 

  • Kavaliers M (1978) Seasonal changes in the circadian period of the lake chub, Couesius plumbeus. Can J Zool 56:2591–2596

    Google Scholar 

  • Kavaliers M (1980) Circadian locomotor activity rhythms of the burbot, Lota lota: seasonal differences in period length and the effect of pinealectomy. J Comp Physiol 136:215–218

    Google Scholar 

  • Kavaliers M (1981) Seasonal effects on the freerunning rhythm of circadian activity of longnose dace (Rhinichthys cataractae). Environ Biol Fish 6:203–206

    Google Scholar 

  • Koilraj AJ, Sharma VK, Marimuthu G, Chandrashekaran MK (2000) Presence of circadian rhythms in the locomotor activity of a cave-dwelling millipede Glyphiulus cavernicolus Sulu (Cambalidae, Spirostreptida). Chronobiol Int 17:757–765

    CAS  PubMed  Google Scholar 

  • Koilraj AJ, Marimuthu G, Sharma VK (1999) Circadian rhythms in the locomotor activity of a surface-dwelling millipede Syngalobolus sp. Biol Rhythm Res 30:529–533

    Google Scholar 

  • Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 68:2112–2116

    CAS  PubMed  Google Scholar 

  • Kronfeld-Schor N, Visser ME, van Gils JA (2017) Chronobiology of interspecific interactions in a changing world. Phil Trans R Soc B 372:20160248. https://doi.org/10.1098/rstb.2016.0248

    Article  PubMed  Google Scholar 

  • Kurosawa G, Goldbeter A (2006) Amplitude of circadian oscillations entrained by 24-h light-dark cycles. J Theoret Biol 242:478–488

    Google Scholar 

  • Kyriacou CP, Peixoto AA, Sandrelli F, Costa R, Tauber E (2008) Clines in clock genes: fine-tuning circadian rhythms to the environment. Trends Genet 24:124–132

    CAS  PubMed  Google Scholar 

  • Laughlin SB, de Ruyter van Steveninck RR, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36–41

    CAS  PubMed  Google Scholar 

  • Lima S, Dill L (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Google Scholar 

  • Lohmann M (1967) Ranges of circadian period length. Experientia 23:788–790

    CAS  PubMed  Google Scholar 

  • Lone SR, Ilangovan V, Murugan M, Sharma VK (2010) Circadian resonance in the development of two sympatric species of Campanotus ants. J Insect Physiol 56:1611–1616

    CAS  PubMed  Google Scholar 

  • Lövei GL, Sunderland KD (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Ann Rev Entomol 41:231–256

    Google Scholar 

  • Lowrey PL, Takahashi JS (2011) Genetics and circadian rhythms in mammalian model organisms. Adv Genet 74:175–230

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martino TA, Oudit GY, Herzenberg AM, Tata N, Koletar MM, Kabir GM, Belsham DD, Backx PH, Ralph MR, Sole MJ (2008) Circadian rhythm disorganization produces profound cardiovascular and renal disease in hamsters. Am J Physiol Regul Integr Comp Physiol 294:R1675–R1683

    CAS  PubMed  Google Scholar 

  • Moore D, Rankin MA (1985) Circadian locomotor rhythms in individual honeybees. Physiol Entomol 10:191–197

    Google Scholar 

  • Moore D, Angel JE, Cheeseman IM, Fahrbach SE, Robinson GE (1998) Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav Ecol Sociobiol 43:147–160

    Google Scholar 

  • Moore D, Watts JC, Herrig A, Jones TC (2016) Exceptionally short-period circadian clock in Cyclosa turbinata: regulation of locomotor and web-building behavior in an orb-weaving spider. J Arachnol 44:388–396

    Google Scholar 

  • Ortega-Escobar J (2002) Circadian rhythms of locomotor activity in Lycosa tarentula (Araneae, Lycosidae) and the pathways of ocular entrainment. Biol Rhythm Res 33:561–576

    Google Scholar 

  • Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci 95:8660–8664

    CAS  PubMed  Google Scholar 

  • Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. I. The stability and lability of spontaneous frequency. J Comp Physiol 106:223–252

    Google Scholar 

  • Pittendrigh CS, Minis DH (1972) Circadian systems: longevity as a function of circadian resonance in Drosophila melanogaster. Proc Nat Acad Sci USA 69:1537–1539

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Press WH, Rybicki GB (1989) Fast algorithm for spectral analysis of unevenly sampled data. Astrophys J 338:277–280

    Google Scholar 

  • Prohaska F, Joplin KH, Moore D (2018) Effects of gender, age, and nutrition on circadian locomotor activity rhythms in the flesh fly Sarcophaga crassipalpis. J Insect Physiol 107:265–275. https://doi.org/10.1016/j.jinsphys.2017.11.007

    Article  CAS  PubMed  Google Scholar 

  • Pruitt JN, DiRenzo N, Kralj-Fišer S, Johnson JC (2011) Individual-and condition-dependent effects on habitat choice and choosiness. Behav Ecol Sociobiol 65:1987–1995

    Google Scholar 

  • Ralph MR, Menaker M (1988) A mutation of the circadian system in golden hamsters. Science 241:1225–1227

    CAS  PubMed  Google Scholar 

  • Ralph MR, Foster RG, Davis FC, Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247:975–978

    CAS  PubMed  Google Scholar 

  • Refinetti R (2012) Integration of biological clocks and rhythms. Compr Physiol 2:1213–1239

    PubMed  Google Scholar 

  • Refinetti R, Wassmer T, Chrukalady R, Pandey VK, Singaravel M, Giannetto C, Piccione G (2016) Variability of behavioral chronotypes of 16 mammalian species under controlled conditions. Physiol Behav 161:53–59

    CAS  PubMed  Google Scholar 

  • Riechert SE, Cady A (1983) Patterns of resource use and tests for competitive release in a spider community. Ecology 64:899–913

    Google Scholar 

  • Ruf T (1999) The Lomb-Scargle periodogram in biological rhythm research: analysis of incomplete and unequally spaced time-series. Biol Rhythm Res 30:178–201

    Google Scholar 

  • Salomon M, Vilbert S, Bennet RG (2010) Habitat use by western black widow spiders (Latrodectus Hesperus) in coastal British Columbia: evidence of facultative group living. Can J Zool 88:334–346

    Google Scholar 

  • Salomon M (2011) The natural diet of a polyphagous predator, Latrodectus hesperus (Araneae: Theridiidae), over one year. J Arachnology 39:154–160

    Google Scholar 

  • Schwartz WJ, Helm B, Gerkema MP (2017) Wild clocks: preface and glossary. Phil Trans R Soc B 372:20170211. https://doi.org/10.1098/rstb.2017.0211

    Article  PubMed  Google Scholar 

  • Seggio JA (2013) The free-running period of Drosophila melanogaster is not affected by the length of the tube in a Drosophila Activity Monitor (DAM). Dro Inf Ser 96:197–199

    Google Scholar 

  • Seyfarth E-A (1980) Daily patterns of locomotor activity in a wandering spider. Physiol Entomol 5:199–206

    Google Scholar 

  • Shemesh Y, Eban-Rothschild A, Cohen M, Bloch G (2010) Molecular dynamics and social regulation of context-dependent plasticity in the circadian clockwork of the honey bee. J Neurosci 30:12517–12525

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu T, Masaki S (1997) Geographical and species variation in circadian rhythm parameters in nemobiine crickets. Physiol Entomol 22:83–93. https://doi.org/10.1111/j.1365-3032.1997.tb01144.x

    Article  Google Scholar 

  • Sokolove PG, Bushell WN (1978) The chi square periodogram: its utility for analysis of circadian rhythms. J Theo Biol 72:131–160

    CAS  Google Scholar 

  • Soriano-Morales S, Caballero-Hernández O, Dávila-Montes M, Morales-Malacara JB, Miranda-Anaya M (2013) Circadian locomotor activity and entrainment by light cycles in cave spiders (Dipluridae and Ctenidae) at the cave Los Riscos. Qro México Bio Rhythm Res 44:949–955

    Google Scholar 

  • Spoelstra K, Wikelski M, Daan S, Loudon ASI, Hau M (2016) Natural selection against a circadian clock gene mutation in mice. Proc Nat Acad Sci USA 113:686–691

    CAS  PubMed  Google Scholar 

  • Steiger SS, Valcu M, Spoelstra K, Helm B, Wikelski M, Kempenaers B (2013) When the sun never sets: diverse activity rhythms under continuous daylight in free-living arctic-breeding birds. Proc Roy Soc B 280:20131016. https://doi.org/10.1098/rspb.2013.1016

    Article  Google Scholar 

  • Suter RB (1993) Circadian rhythmicity and other patterns of spontaneous motor activity in Frontinella pyramitela (Linyphiidae) and Argyrodes trigonum (Theridiidae). J Arachnol 21:6–22

    Google Scholar 

  • Suter RB, Benson K (2014) Nocturnal, diurnal, crepuscular: activity assessments of Pisauridae and Lycosidae. J Arachnology 42:178–191

    Google Scholar 

  • Tomioka K, Uwozumi K, Matsumoto N (1997) Light cycles given during development affect freerunning period of circadian locomotor rhythm of period mutants in Drosophila melanogaster. J Insect Physiol 43:297–305

    CAS  PubMed  Google Scholar 

  • Turek FW (2008) Staying off the dance floor: when no rhythm is better than bad rhythm. Am J Physiol Regul Integr Comp Physiol 294:R1672–1674

    CAS  PubMed  Google Scholar 

  • Van der Veen DR, Gerkema MP (2017) Unmasking ultradian rhythms in gene expression. FASEB J 31:743–750

    PubMed  Google Scholar 

  • Van Dongen H, Olofsen E, VanHartevelt JH, Kruyt EW (1999) Searching for biological rhythms: peak detection in the periodogram of unequally spaced data. J Biol Rhythms 14:617–620

    PubMed  Google Scholar 

  • Vaze KM, Helfrich-Förster C (2016) Drosophila ezoana uses an hour-glass or highly damped circadian clock for measuring night length and inducing diapause. Physiol Entomol 41:378–389

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vitaterna MH, Ko CH, Chang A-M, Buhr ED, Freuchte EM, Schook A, Antoch MP, Turek FW, Takahashi JS (2006) The mouse Clock mutation reduces circadian pacemaker amplitude and enhances efficacy of resetting stimuli and phase-response curve amplitude. Proc Nat Acad Sci USA 103:9327–9332

    CAS  PubMed  Google Scholar 

  • von Saint PU, Aschoff J (1978) Longevity among blowflies Phormia terraenovae R.D. kept in non-24-hour light-dark cycles. J Comp Physiol 127:191–195

    Google Scholar 

  • Watts JC, Ross C, Jones TC (2015) Diel and life-history characteristics of personality: consistency versus flexibility in relation to ecological change. Anim Behav 101:43–49

    Google Scholar 

  • Wise DH (1993) Spiders in ecological webs. Cambridge University Press, Cambridge

    Google Scholar 

  • Woelfle MA, Ouyang Y, Phanvijhitsiri K, Johnson KH (2004) The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Curr Biol 14:1481–1486

    CAS  PubMed  Google Scholar 

  • Wyse C, Coogan A, Selman C, Hazlerigg D, Speakman J (2010) Association between mammalian lifespan and circadian free-running period: the circadian resonance hypothesis revisited. Biol Lett 6:696–698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi Y, Suzuki T, Mizoro Y, Kori H, Okada K, Chen Y, Fustin J-M, Yamazaki F, Mizuguchi N, Zhang J, Dong X, Tsujimoto G, Okuno Y, Doi M, Okamura H (2013) Mice genetically deficient in vasopressin V1a and V1b receptors are resistant to jet lag. Science 342:85–90

    CAS  PubMed  Google Scholar 

  • Zakharenko LP, Pterovskii DV, Putilov AA (2018) Larks, owls, swifts, and woodcocks among fruit flies: differential responses of four heritable chronotypes to long and hot summer days. Nat Sci Sleep 10:181–191

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We gratefully acknowledge support from the National Science Foundation (IOS Grant No. 1257133). We additionally acknowledge support from the Washington and Lee University Summer Scholar’s Program. We thank the ETSU Department of Biological Sciences for logistical support and M. Miller, R. Wilson, and M. Gauck for assistance in collecting spiders. Finally, we thank F. Barth, B. Helm, and an anonymous reviewer for their exceptionally helpful comments on this manuscript. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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  1. Center for Neural Science, New York University, 4 Washington Pl #809, New York, NY, 10003, USA

    Andrew Mah

  2. Department of Biology, Washington and Lee University, Howe Hall, Lexington, VA, 24450, USA

    Nadia Ayoub & Natalia Toporikova

  3. Neuroscience Program, Washington and Lee University, 204 W. Washington Street, Lexington, VA, 24450, USA

    Natalia Toporikova

  4. Department of Biological Sciences, East Tennessee State University, Box 70703, Johnson City, TN, 37604, USA

    Thomas C. Jones & Darrell Moore

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Mah, A., Ayoub, N., Toporikova, N. et al. Locomotor activity patterns in three spider species suggest relaxed selection on endogenous circadian period and novel features of chronotype. J Comp Physiol A 206, 499–515 (2020). https://doi.org/10.1007/s00359-020-01412-y

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