- Email: [email protected]
Sleep: Never Wasted but Often Too Short
Current Biology
Dispatches neural crest cells are mesenchymal whereas follicle cells are epithelial. It has been suggested that collective migration of mesenchymal and epithelial cells could use different mechanisms [17], but the work by Stedden et al. [11] indicates that these two cell types share CIL as the driving force to polarize the collective. This work also sheds light on the principles behind CIL, as it shows that this process can be present in a group of cells that exhibit protrusions pointing in the same direction of migration, as has been described for chick neural crest [18]. It will be interesting to know whether other collectively migrating cells use CIL as one of the mechanisms to coordinate their migration, even if the molecular mechanism of this CIL differs in other systems [19]. While this work demonstrates a definitive role for Semaphorins and Plexins in collective cell migration, it also raises some questions. The model works nicely to transmit planar cell polarity from a cell that is already polarized, but how is the polarization established in the first place? Is the Semaphorin–Plexin interaction a mechanism to initiate polarity or to amplify a previously existing polarity? Despite these questions, we can confidently say that, similar to the repulsion between locusts that is based on cannibalistic behaviour and is essential for collective migration [20], cell repulsion is indispensable for the collective migration of cells.
REFERENCES 1. Couzin, I.D. (2018). Collective animal migration. Curr. Biol. 28, R976–R980. 2. Ladoux, B., and Me`ge, R.M. (2017). Mechanobiology of collective cell behaviours. Nat. Rev. Mol. Cell Biol. 18, 743–757. 3. Mayor, R., and Etienne-Manneville, S. (2016). The front and rear of collective cell migration. Nat. Rev. Mol. Cell Biol. 17, 97–109. 4. Haeger, A., Wolf, K., Zegers, M.M., and Friedl, P. (2015). Collective cell migration: guidance principles and hierarchies. Trends Cell Biol. 25, 556–566. 5. Scarpa, E., and Mayor, R. (2016). Collective cell migration in development. J. Cell Biol. 212, 143–155. 6. Berdahl, A.M., Kao, A.B., Flack, A., Westley, P.A.H., Codling, E.A., Couzin, I.D., Dell, A.I., and Biro, D. (2018). Collective animal navigation and migratory culture: from theoretical models to empirical evidence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 373, https://doi.org/10.1098/rstb.2017.0009.
hes, E., and Vicsek, T. (2014). Collective 7. Me motion of cells: from experiments to models. Integr. Biol. 6, 831–854. 8. Szabo´, A., and Mayor, R. (2016). Modelling collective cell migration of neural crest. Curr. Opin. Cell Biol. 42, 22–28. 9. Carmona-Fontaine, C., Matthews, H.K., Kuriyama, S., Moreno, M., Dunn, G.A., Parsons, M., Stern, C.D., and Mayor, R. (2008). Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456, 957–956. 10. Horne-Badovinac, S. (2014). The Drosophila egg chamber—a new spin on how tissues elongate. Integr. Comp. Biol. 54, 667–676. 11. Stedden, C.G., Menegas, W., Zajac, A.L., Williams, A.M., Cheng, S., O¨zkan, E., and Horne-Badovinac, S. (2019). Planar-polarized Semaphorin-5c and Plexin A promote the collective migration of epithelial cells in Drosophila. Curr. Biol. 29, 908–920. 12. Alto, L.T., and Terman, J.R. (2017). Semaphorins and their signaling mechanisms. Methods Mol. Biol. 1493, 1–25. 13. Cetera, M., Ramirez-San Juan, G.R., Oakes, P.W., Lewellyn, L., Fairchild, M.J., Tanentzapf, G., Gardel, M.L., and Horne-Badovinac, S. (2014). Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation. Nat. Commun. 5, 5511.
14. Negishi, M., Oinuma, I., and Katoh, H. (2005). Plexins: axon guidance and signal transduction. Cell Mol. Life Sci. 62, 1363– 1371. 15. Gurrapu, S., and Tamagnone, L. (2016). Transmembrane semaphorins: Multimodal signaling cues in development and cancer. Cell Adh. Migr. 10, 675–691. 16. Barlan, K., Cetera, M., and Horne-Badovinac, S. (2017). Fat2 and Lar define a basally localized planar signaling system controlling collective cell migration. Dev. Cell 40, 467– 477.e5. 17. Theveneau, E., and Mayor, R. (2013). Collective cell migration of epithelial and mesenchymal cells. Cell Mol. Life Sci. 70, 3481–3492. 18. Genuth, M.A., Allen, C.D.C., Mikawa, T., and Weiner, O.D. (2018). Chick cranial neural crest cells use progressive polarity refinement, not contact inhibition of locomotion, to guide their migration. Dev. Biol., S0012-1606(17) 30654–1. 19. Stramer, B., and Mayor, R. (2017). Mechanisms and in vivo functions of contact inhibition of locomotion. Nat. Rev. Mol. Cell Biol. 18, 43–55. 20. Bazazi, S., Buhl, J., Hale, J.J., Anstey, M.L., Sword, G.A., Simpson, S.J., and Couzin, I.D. (2008). Collective motion and cannibalism in locust migratory bands. Curr. Biol. 18, 735–739.
Sleep: Never Wasted but Often Too Short Thomas Kantermann1,2 1University of Applied Sciences for Economics and Management (FOM), Hammfelddamm 2, 41460 Neuss, Germany 2SynOpus, Alte Hattinger Strasse 32, 44789 Bochum, Germany Correspondence: [email protected] https://doi.org/10.1016/j.cub.2018.12.030
Sleep duration and food intake are interconnected and important for health. New research shows that reducing sleep across five nights leads to more snacking after dinner and metabolic disturbances, which ad libitum weekend sleep could only partially compensate for. The weekend: the end-of-the-week island of liberty and freedom. Weekends provide room to recover from the workweek, offering time for extended leisure activities with friends and family, and — perhaps most treasured of all — more time to sleep. It is not an understatement that weekends, for
many people, are a sleep refuge. Epidemiological research shows that about 35% of American adults on average sleep less than seven hours per night [1] and about another third sleep fewer than six hours per night. Specific demographic groups sleep even less, for instance, active military personnel who
Current Biology 29, R200–R223, March 18, 2019 ª 2018 Elsevier Ltd. R207
Current Biology
Dispatches in over 40% of cases sleep not more than five hours per night [2–4]. And lack of sufficient sleep comes at significant health costs. In a 2017 study [5], Akerstedt and colleagues presented data collected from 43,880 subjects over 13 years showing a 52% higher mortality rate in individuals younger than 65 years who slept less than or equal to five hours per night during weekends. The good news, which was elaborated in the same study [5], is that longer sleep on weekends seems to secure health. The mortality rate in individuals sleeping fewer hours during weekdays but sleeping longer during weekends did not differ from the mortality rate of individuals with seven hours sleep per night [5] throughout the week. Longer sleep equal to or more than nine hours on weekend nights was not associated with increased mortality [5]. The authors conclude that long weekend sleep may possibly help compensate for insufficient sleep during the week [5]. And, indeed, the only solution to reduce the costs of lost sleep is to sleep longer after sleep loss has occurred and not before. This is because evolution has not equipped humans with the capacity to bank sleep, that is, to store sleep like we store electric energy in a battery [6]. The bottom line is, yes, weekends can help compensate for insufficient weekday sleep. But, only to some extent, as a newly published paper by Depner and colleagues [7] in this issue of Current Biology now shows. In a sophisticated laboratory study, Depner and colleagues [7] investigated the question whether metabolic disturbances that result from recurrent insufficient sleep is prevented through ad libitum weekend recovery sleep. The authors assessed sleep, circadian timing of melatonin, energy intake, body weight, and insulin sensitivity in three randomised groups across nine nights: a control group with nine hours of sleep each night; a sleep restriction (SR) group with five hours of sleep and with no recovery sleep; and a sleep restriction group with ad libitum recovery sleep (WR) on a two-day weekend, followed by another two nights of, again, insufficient sleep. Compared to the control group, the SR and WR groups with insufficient sleep increased energy intake and body weight from snacking after dinner. Ad libitum weekend recovery
sleep led to about one hour more of sleep and a decrease in after-dinner energy intake compared to the days with insufficient sleep [7]. Furthermore, Depner and colleagues [7] found that, during the days of subsequent forced sleep restriction (following the simulated recovery ad libitum sleep weekend), the circadian phase of melatonin in their participants was delayed, and energy intake after dinner as well as body weight increased compared to baseline values. The participants in the SR group without recovery weekend sleep showed decreased whole-body insulin sensitivity by about 13% during the days of insufficient sleep compared to the baseline days. The participants in the WR group showed a decrease in whole-body, hepatic, and muscle insulin sensitivity of about 9 to 27% during the days of recurrent insufficient sleep compared to the baseline days. With respect to participant sex, while women slept more during the weekend recovery, as expected, the total sleep duration was still less than that seen in men. And, with regard to energy intake, while men exhibited reduced energy intake during the recovery weekend, women ate even less, their energy intake returning to baseline levels [7]. These findings led the authors to conclude that recovery sleep on weekends does not help prevent metabolic disturbances in connection with insufficient sleep during the workweek [7]. This conclusion is in contrast to the conclusion of Akerstedt and colleagues [5], but in line with other research showing that weekend recovery sleep did not help improve objective performance deficits, albeit positive effects on daytime sleepiness, fatigue, IL-6 levels and cortisol were reported [8]. Another example is a study by Huang et al. [9] showing that weekend catch-up only in combination with more physical activity reduced the risk of childhood obesity. One might be tempted to say that Depner and colleagues [7] show that the human body does not store sleep but sleep-loss related energy in form of increased body weight. Although an untested hypothesis, for individuals who find it challenging to maintain weight for health reasons, a period of carefully controlled (mild) sleep deprivation might
R208 Current Biology 29, R200–R223, March 18, 2019
help them gain more weight. Other positive effects of sleep deprivation have, for example, been shown in the treatment of depression [10]. For all others, however, these findings are worrisome. Depner and colleagues [7] cite results of the Global Burden of Disease study showing that in 2015 about 603.7 million adults were obese [11]. And, high body mass index is one of the main reasons leading to cardiovascular disease and diabetes [11]. As mentioned above, in addition to the changes in sleep duration, energy intake, weight-gain and insulin sensitivity, Depner and colleagues [7] also report a delay in the circadian phase of melatonin over the weekend. This finding fits with an earlier study by Crowley and Carskadon in adolescents who also exhibited a delayed circadian phase, again measured by melatonin, over the weekend [12]. The authors in their study [12] tested the ability of light exposure in the morning to prevent the phase delay of melatonin, but this was ineffective. A more recent study by Zerbini and co-workers [13] also showed that increased morning light exposure is ineffective with respect to circadian phase shifts on both workdays and workfree days. But, reducing light exposure in the evening helped advance both the circadian phase of melatonin and sleep onset on workdays [13]. The phase advancing effect of reduced evening light exposure in combination with more daylight exposure all day long on both sleep timing and melatonin has also been shown in an earlier study by Stothard and colleagues [14]. These findings, taken together, underline that the circadian phase is not a stable trait independent of environmental conditions. It has been shown that circadian markers are best reproducible when environmental conditions remain stable [15] and that sleep timing on work-free days (weekends), as opposed to workdays, is not necessarily correlated best with the circadian phase of melatonin [16]. To what extent tailored light interventions could help improve recovery on weekends and stabilise circadian phase, however, still demands more research. In conclusion, the findings by Depner and colleagues [7] show that alternating between different sleep behaviours during the workweek and weekend coincides with metabolic disturbances,
Current Biology
Dispatches changes in eating behaviour and shifts in the circadian phase of melatonin. Extreme forms of similar disturbances concern shift- and night workers, whose physiology often is significantly compromised [17–19]. Further research is needed to explore, for example, how long healthy recovery sleep periods ideally should be, especially in different sexes and populations like young children and their parents, adolescents, shift workers and individuals with health problems [20]. At the end of the day, of course, none of this should discourage anyone from looking forward to the weekend, but it most likely is too short for sufficient recovery at all levels. Hence, one might feel encouraged to not necessarily wait for the end of the week to finally sleep. Whichever day of the week, sleep is never wasted. REFERENCES 1. Centers for Disease Control and Prevention. (2014). Short Sleep Duration Among US. Adults.
9. Huang, W.Y., and Wong, S.H.S. (2018). Prospective associations between weekend catch-up sleep, physical activity, and childhood obesity. Child. Obes. 15, 40–47.
15. Kantermann, T., and Eastman, C.I. (2018). Circadian phase, circadian period and chronotype are reproducible over months. Chronobiol. Int. 35, 280–288.
10. Boland, E.M., Rao, H., Dinges, D.F., Smith, R.V., Goel, N., Detre, J.A., Basner, M., Sheline, Y.I., Thase, M.E., and Gehrman, P.R. (2017). Meta-analysis of the antidepressant effects of acute sleep deprivation. J. Clin. Psychiatry 8, e1020–e1034.
16. Kantermann, T., and Burgess, H.J. (2017). Average mid-sleep time as a proxy for circadian phase. Psych. J. 6, 290–291.
11. Afshin, A., Reitsma, M.B., and Murray, C.J.L. (2017). Health effects of overweight and obesity in 195 countries. N. Engl. J. Med. 15, 1496–1497. 12. Crowley, S.J., and Carskadon, M.A. (2010). Modifications to weekend recovery sleep delay circadian phase in older adolescents. Chronobiol. Int. 7, 1469–1492. 13. Zerbini, G., Kantermann, T., and Merrow, M. (2018). Strategies to decrease social jetlag: reducing evening blue light advances sleep and melatonin. Eur. J. Neurosci., In Press. https://doi.org/10.1111/ejn.14293. 14. Stothard, E.R., McHill, A.W., Depner, C.M., Birks, B.R., Moehlman, T.M., Ritchie, H.K., Guzzetti, J.R., Chinoy, E.D., LeBourgeois, M.K., Axelsson, J., et al. (2017). Circadian entrainment to the natural light-dark cycle across seasons and the weekend. Curr. Biol. 27, 508–513.
17. Rotter, M., Brandmaier, S., Covic, M., Burek, K., Hertel, J., Troll, M., Bader, E., Adam, J., Prehn, C., Rathkolb, B., et al. (2018). Night shift work affects urine metabolite profiles of nurses with early chronotype. Metabolites 8, 45. 18. Kantermann, T., Wehrens, S.M., Ulhoa, M.A., Moreno, C., and Skene, D.J. (2012). Noisy and individual, but doable: shift-work research in humans. Prog. Brain Res. 199, 399–411. 19. Kervezee, L., Kosmadopoulos, A., and Boivin, D.B. (2018). Metabolic and cardiovascular consequences of shift work: The role of circadian disruption and sleep disturbances. Eur. J. Neurosci., In Press. https://doi.org/10. 1111/ejn.14216. 20. Gershon, A., Johnson, S.L., Thomas, L., and Singh, M.K. (2018). Double trouble: weekend sleep changes are associated with increased impulsivity among adolescents with bipolar I disorder. Bipolar Disord., In Press. https://doi. org/10.1111/bdi.12658.
2. Centers for Disease Control and Prevention (CDC). (2011). Effect of short sleep duration on daily activities–United States, 2005–2008. MMWR. Morb. Mortal. Wkly. Rep. 8, 239–242. 3. Ford, E.S., Cunningham, T.J., and Croft, J.B. (2015). Trends in self-reported sleep duration among US adults from 1985 to 2012. Sleep 5, 829–832. 4. Mysliwiec, V., McGraw, L., Pierce, R., Smith, P., Trapp, B., and Roth, B.J. (2013). Sleep disorders and associated medical comorbidities in active duty military personnel. Sleep 2, 167–174. 5. Akerstedt, T., Ghilotti, F., Grotta, A., Zhao, H., Adami, H.O., Trolle-Lagerros, Y., and Bellocco, R. (2018). Sleep duration and mortality - Does weekend sleep matter? J. Sleep Res. 28, e12712. 6. Rupp, T.L., Wesensten, N.J., Bliese, P.D., and Balkin, T.J. (2009). Banking sleep: realization of benefits during subsequent sleep restriction and recovery. Sleep 3, 311–321. 7. Depner, C.M., Melanson, E.L., Eckel, R.H., Snell-Bergeon, J.K., Perreault, L., Bergman, B.C., Higgins, J.A., Guerin, M.K., Stothard, E.R., Morton, S.J., and Wright, K.P. (2019). Ad libitum weekend recovery sleep fails to prevent metabolic dysregulation during a repeating pattern of insufficient sleep and weekend recovery sleep. Curr. Biol. 29, 957–967. 8. Pejovic, S., Basta, M., Vgontzas, A.N., Kritikou, I., Shaffer, M.L., Tsaoussoglou, M., Stiffler, D., Stefanakis, Z., Bixler, E.O., and Chrousos, G.P. (2013). Effects of recovery sleep after one work week of mild sleep restriction on interleukin-6 and cortisol secretion and daytime sleepiness and performance. Am. J. Physiol. Endocrinol. Metab. 7, E890– E896.
Biotremology: We Fight for Food Peggy S.M. Hill Professor Emerita, Department of Biological Science, The University of Tulsa, Tulsa, OK 74015, USA Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.01.061
A new study shines light on an already well-known and mutually beneficial association between ants and the acacia tree. For the first time in this system, plant-borne vibrations introduced by foraging browsers are confirmed as the cue that directs ants to attack the attacker. Most of us know that living things on our planet sometimes form associations with others outside their species, a symbiosis like that of corals in a reef and the algae that give coral its beautiful coloration. We learn this in secondary and college-level textbooks, but also from nature films and online videos, and even from Nemo and the sea anemone. In the USA the term mutualism refers to the type of symbiosis in which both species benefit from the association. This is contrasted with the
other two symbioses: parasitism, where one benefits while the other is harmed (+-), and commensalism, where one benefits and the other is not helped or harmed (+0), as when flying sea birds are incidentally helped to catch fish that have fled to near the surface to escape being eaten by bigger fish. The sea birds benefit from feasting on an aggregation of prey that might otherwise have been inaccessible in deeper water, while the bigger fish are not affected by the sea
Current Biology 29, R200–R223, March 18, 2019 ª 2019 Elsevier Ltd. R209
Dispatches neural crest cells are mesenchymal whereas follicle cells are epithelial. It has been suggested that collective migration of mesenchymal and epithelial cells could use different mechanisms [17], but the work by Stedden et al. [11] indicates that these two cell types share CIL as the driving force to polarize the collective. This work also sheds light on the principles behind CIL, as it shows that this process can be present in a group of cells that exhibit protrusions pointing in the same direction of migration, as has been described for chick neural crest [18]. It will be interesting to know whether other collectively migrating cells use CIL as one of the mechanisms to coordinate their migration, even if the molecular mechanism of this CIL differs in other systems [19]. While this work demonstrates a definitive role for Semaphorins and Plexins in collective cell migration, it also raises some questions. The model works nicely to transmit planar cell polarity from a cell that is already polarized, but how is the polarization established in the first place? Is the Semaphorin–Plexin interaction a mechanism to initiate polarity or to amplify a previously existing polarity? Despite these questions, we can confidently say that, similar to the repulsion between locusts that is based on cannibalistic behaviour and is essential for collective migration [20], cell repulsion is indispensable for the collective migration of cells.
REFERENCES 1. Couzin, I.D. (2018). Collective animal migration. Curr. Biol. 28, R976–R980. 2. Ladoux, B., and Me`ge, R.M. (2017). Mechanobiology of collective cell behaviours. Nat. Rev. Mol. Cell Biol. 18, 743–757. 3. Mayor, R., and Etienne-Manneville, S. (2016). The front and rear of collective cell migration. Nat. Rev. Mol. Cell Biol. 17, 97–109. 4. Haeger, A., Wolf, K., Zegers, M.M., and Friedl, P. (2015). Collective cell migration: guidance principles and hierarchies. Trends Cell Biol. 25, 556–566. 5. Scarpa, E., and Mayor, R. (2016). Collective cell migration in development. J. Cell Biol. 212, 143–155. 6. Berdahl, A.M., Kao, A.B., Flack, A., Westley, P.A.H., Codling, E.A., Couzin, I.D., Dell, A.I., and Biro, D. (2018). Collective animal navigation and migratory culture: from theoretical models to empirical evidence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 373, https://doi.org/10.1098/rstb.2017.0009.
hes, E., and Vicsek, T. (2014). Collective 7. Me motion of cells: from experiments to models. Integr. Biol. 6, 831–854. 8. Szabo´, A., and Mayor, R. (2016). Modelling collective cell migration of neural crest. Curr. Opin. Cell Biol. 42, 22–28. 9. Carmona-Fontaine, C., Matthews, H.K., Kuriyama, S., Moreno, M., Dunn, G.A., Parsons, M., Stern, C.D., and Mayor, R. (2008). Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456, 957–956. 10. Horne-Badovinac, S. (2014). The Drosophila egg chamber—a new spin on how tissues elongate. Integr. Comp. Biol. 54, 667–676. 11. Stedden, C.G., Menegas, W., Zajac, A.L., Williams, A.M., Cheng, S., O¨zkan, E., and Horne-Badovinac, S. (2019). Planar-polarized Semaphorin-5c and Plexin A promote the collective migration of epithelial cells in Drosophila. Curr. Biol. 29, 908–920. 12. Alto, L.T., and Terman, J.R. (2017). Semaphorins and their signaling mechanisms. Methods Mol. Biol. 1493, 1–25. 13. Cetera, M., Ramirez-San Juan, G.R., Oakes, P.W., Lewellyn, L., Fairchild, M.J., Tanentzapf, G., Gardel, M.L., and Horne-Badovinac, S. (2014). Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation. Nat. Commun. 5, 5511.
14. Negishi, M., Oinuma, I., and Katoh, H. (2005). Plexins: axon guidance and signal transduction. Cell Mol. Life Sci. 62, 1363– 1371. 15. Gurrapu, S., and Tamagnone, L. (2016). Transmembrane semaphorins: Multimodal signaling cues in development and cancer. Cell Adh. Migr. 10, 675–691. 16. Barlan, K., Cetera, M., and Horne-Badovinac, S. (2017). Fat2 and Lar define a basally localized planar signaling system controlling collective cell migration. Dev. Cell 40, 467– 477.e5. 17. Theveneau, E., and Mayor, R. (2013). Collective cell migration of epithelial and mesenchymal cells. Cell Mol. Life Sci. 70, 3481–3492. 18. Genuth, M.A., Allen, C.D.C., Mikawa, T., and Weiner, O.D. (2018). Chick cranial neural crest cells use progressive polarity refinement, not contact inhibition of locomotion, to guide their migration. Dev. Biol., S0012-1606(17) 30654–1. 19. Stramer, B., and Mayor, R. (2017). Mechanisms and in vivo functions of contact inhibition of locomotion. Nat. Rev. Mol. Cell Biol. 18, 43–55. 20. Bazazi, S., Buhl, J., Hale, J.J., Anstey, M.L., Sword, G.A., Simpson, S.J., and Couzin, I.D. (2008). Collective motion and cannibalism in locust migratory bands. Curr. Biol. 18, 735–739.
Sleep: Never Wasted but Often Too Short Thomas Kantermann1,2 1University of Applied Sciences for Economics and Management (FOM), Hammfelddamm 2, 41460 Neuss, Germany 2SynOpus, Alte Hattinger Strasse 32, 44789 Bochum, Germany Correspondence: [email protected] https://doi.org/10.1016/j.cub.2018.12.030
Sleep duration and food intake are interconnected and important for health. New research shows that reducing sleep across five nights leads to more snacking after dinner and metabolic disturbances, which ad libitum weekend sleep could only partially compensate for. The weekend: the end-of-the-week island of liberty and freedom. Weekends provide room to recover from the workweek, offering time for extended leisure activities with friends and family, and — perhaps most treasured of all — more time to sleep. It is not an understatement that weekends, for
many people, are a sleep refuge. Epidemiological research shows that about 35% of American adults on average sleep less than seven hours per night [1] and about another third sleep fewer than six hours per night. Specific demographic groups sleep even less, for instance, active military personnel who
Current Biology 29, R200–R223, March 18, 2019 ª 2018 Elsevier Ltd. R207
Current Biology
Dispatches in over 40% of cases sleep not more than five hours per night [2–4]. And lack of sufficient sleep comes at significant health costs. In a 2017 study [5], Akerstedt and colleagues presented data collected from 43,880 subjects over 13 years showing a 52% higher mortality rate in individuals younger than 65 years who slept less than or equal to five hours per night during weekends. The good news, which was elaborated in the same study [5], is that longer sleep on weekends seems to secure health. The mortality rate in individuals sleeping fewer hours during weekdays but sleeping longer during weekends did not differ from the mortality rate of individuals with seven hours sleep per night [5] throughout the week. Longer sleep equal to or more than nine hours on weekend nights was not associated with increased mortality [5]. The authors conclude that long weekend sleep may possibly help compensate for insufficient sleep during the week [5]. And, indeed, the only solution to reduce the costs of lost sleep is to sleep longer after sleep loss has occurred and not before. This is because evolution has not equipped humans with the capacity to bank sleep, that is, to store sleep like we store electric energy in a battery [6]. The bottom line is, yes, weekends can help compensate for insufficient weekday sleep. But, only to some extent, as a newly published paper by Depner and colleagues [7] in this issue of Current Biology now shows. In a sophisticated laboratory study, Depner and colleagues [7] investigated the question whether metabolic disturbances that result from recurrent insufficient sleep is prevented through ad libitum weekend recovery sleep. The authors assessed sleep, circadian timing of melatonin, energy intake, body weight, and insulin sensitivity in three randomised groups across nine nights: a control group with nine hours of sleep each night; a sleep restriction (SR) group with five hours of sleep and with no recovery sleep; and a sleep restriction group with ad libitum recovery sleep (WR) on a two-day weekend, followed by another two nights of, again, insufficient sleep. Compared to the control group, the SR and WR groups with insufficient sleep increased energy intake and body weight from snacking after dinner. Ad libitum weekend recovery
sleep led to about one hour more of sleep and a decrease in after-dinner energy intake compared to the days with insufficient sleep [7]. Furthermore, Depner and colleagues [7] found that, during the days of subsequent forced sleep restriction (following the simulated recovery ad libitum sleep weekend), the circadian phase of melatonin in their participants was delayed, and energy intake after dinner as well as body weight increased compared to baseline values. The participants in the SR group without recovery weekend sleep showed decreased whole-body insulin sensitivity by about 13% during the days of insufficient sleep compared to the baseline days. The participants in the WR group showed a decrease in whole-body, hepatic, and muscle insulin sensitivity of about 9 to 27% during the days of recurrent insufficient sleep compared to the baseline days. With respect to participant sex, while women slept more during the weekend recovery, as expected, the total sleep duration was still less than that seen in men. And, with regard to energy intake, while men exhibited reduced energy intake during the recovery weekend, women ate even less, their energy intake returning to baseline levels [7]. These findings led the authors to conclude that recovery sleep on weekends does not help prevent metabolic disturbances in connection with insufficient sleep during the workweek [7]. This conclusion is in contrast to the conclusion of Akerstedt and colleagues [5], but in line with other research showing that weekend recovery sleep did not help improve objective performance deficits, albeit positive effects on daytime sleepiness, fatigue, IL-6 levels and cortisol were reported [8]. Another example is a study by Huang et al. [9] showing that weekend catch-up only in combination with more physical activity reduced the risk of childhood obesity. One might be tempted to say that Depner and colleagues [7] show that the human body does not store sleep but sleep-loss related energy in form of increased body weight. Although an untested hypothesis, for individuals who find it challenging to maintain weight for health reasons, a period of carefully controlled (mild) sleep deprivation might
R208 Current Biology 29, R200–R223, March 18, 2019
help them gain more weight. Other positive effects of sleep deprivation have, for example, been shown in the treatment of depression [10]. For all others, however, these findings are worrisome. Depner and colleagues [7] cite results of the Global Burden of Disease study showing that in 2015 about 603.7 million adults were obese [11]. And, high body mass index is one of the main reasons leading to cardiovascular disease and diabetes [11]. As mentioned above, in addition to the changes in sleep duration, energy intake, weight-gain and insulin sensitivity, Depner and colleagues [7] also report a delay in the circadian phase of melatonin over the weekend. This finding fits with an earlier study by Crowley and Carskadon in adolescents who also exhibited a delayed circadian phase, again measured by melatonin, over the weekend [12]. The authors in their study [12] tested the ability of light exposure in the morning to prevent the phase delay of melatonin, but this was ineffective. A more recent study by Zerbini and co-workers [13] also showed that increased morning light exposure is ineffective with respect to circadian phase shifts on both workdays and workfree days. But, reducing light exposure in the evening helped advance both the circadian phase of melatonin and sleep onset on workdays [13]. The phase advancing effect of reduced evening light exposure in combination with more daylight exposure all day long on both sleep timing and melatonin has also been shown in an earlier study by Stothard and colleagues [14]. These findings, taken together, underline that the circadian phase is not a stable trait independent of environmental conditions. It has been shown that circadian markers are best reproducible when environmental conditions remain stable [15] and that sleep timing on work-free days (weekends), as opposed to workdays, is not necessarily correlated best with the circadian phase of melatonin [16]. To what extent tailored light interventions could help improve recovery on weekends and stabilise circadian phase, however, still demands more research. In conclusion, the findings by Depner and colleagues [7] show that alternating between different sleep behaviours during the workweek and weekend coincides with metabolic disturbances,
Current Biology
Dispatches changes in eating behaviour and shifts in the circadian phase of melatonin. Extreme forms of similar disturbances concern shift- and night workers, whose physiology often is significantly compromised [17–19]. Further research is needed to explore, for example, how long healthy recovery sleep periods ideally should be, especially in different sexes and populations like young children and their parents, adolescents, shift workers and individuals with health problems [20]. At the end of the day, of course, none of this should discourage anyone from looking forward to the weekend, but it most likely is too short for sufficient recovery at all levels. Hence, one might feel encouraged to not necessarily wait for the end of the week to finally sleep. Whichever day of the week, sleep is never wasted. REFERENCES 1. Centers for Disease Control and Prevention. (2014). Short Sleep Duration Among US. Adults.
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11. Afshin, A., Reitsma, M.B., and Murray, C.J.L. (2017). Health effects of overweight and obesity in 195 countries. N. Engl. J. Med. 15, 1496–1497. 12. Crowley, S.J., and Carskadon, M.A. (2010). Modifications to weekend recovery sleep delay circadian phase in older adolescents. Chronobiol. Int. 7, 1469–1492. 13. Zerbini, G., Kantermann, T., and Merrow, M. (2018). Strategies to decrease social jetlag: reducing evening blue light advances sleep and melatonin. Eur. J. Neurosci., In Press. https://doi.org/10.1111/ejn.14293. 14. Stothard, E.R., McHill, A.W., Depner, C.M., Birks, B.R., Moehlman, T.M., Ritchie, H.K., Guzzetti, J.R., Chinoy, E.D., LeBourgeois, M.K., Axelsson, J., et al. (2017). Circadian entrainment to the natural light-dark cycle across seasons and the weekend. Curr. Biol. 27, 508–513.
17. Rotter, M., Brandmaier, S., Covic, M., Burek, K., Hertel, J., Troll, M., Bader, E., Adam, J., Prehn, C., Rathkolb, B., et al. (2018). Night shift work affects urine metabolite profiles of nurses with early chronotype. Metabolites 8, 45. 18. Kantermann, T., Wehrens, S.M., Ulhoa, M.A., Moreno, C., and Skene, D.J. (2012). Noisy and individual, but doable: shift-work research in humans. Prog. Brain Res. 199, 399–411. 19. Kervezee, L., Kosmadopoulos, A., and Boivin, D.B. (2018). Metabolic and cardiovascular consequences of shift work: The role of circadian disruption and sleep disturbances. Eur. J. Neurosci., In Press. https://doi.org/10. 1111/ejn.14216. 20. Gershon, A., Johnson, S.L., Thomas, L., and Singh, M.K. (2018). Double trouble: weekend sleep changes are associated with increased impulsivity among adolescents with bipolar I disorder. Bipolar Disord., In Press. https://doi. org/10.1111/bdi.12658.
2. Centers for Disease Control and Prevention (CDC). (2011). Effect of short sleep duration on daily activities–United States, 2005–2008. MMWR. Morb. Mortal. Wkly. Rep. 8, 239–242. 3. Ford, E.S., Cunningham, T.J., and Croft, J.B. (2015). Trends in self-reported sleep duration among US adults from 1985 to 2012. Sleep 5, 829–832. 4. Mysliwiec, V., McGraw, L., Pierce, R., Smith, P., Trapp, B., and Roth, B.J. (2013). Sleep disorders and associated medical comorbidities in active duty military personnel. Sleep 2, 167–174. 5. Akerstedt, T., Ghilotti, F., Grotta, A., Zhao, H., Adami, H.O., Trolle-Lagerros, Y., and Bellocco, R. (2018). Sleep duration and mortality - Does weekend sleep matter? J. Sleep Res. 28, e12712. 6. Rupp, T.L., Wesensten, N.J., Bliese, P.D., and Balkin, T.J. (2009). Banking sleep: realization of benefits during subsequent sleep restriction and recovery. Sleep 3, 311–321. 7. Depner, C.M., Melanson, E.L., Eckel, R.H., Snell-Bergeon, J.K., Perreault, L., Bergman, B.C., Higgins, J.A., Guerin, M.K., Stothard, E.R., Morton, S.J., and Wright, K.P. (2019). Ad libitum weekend recovery sleep fails to prevent metabolic dysregulation during a repeating pattern of insufficient sleep and weekend recovery sleep. Curr. Biol. 29, 957–967. 8. Pejovic, S., Basta, M., Vgontzas, A.N., Kritikou, I., Shaffer, M.L., Tsaoussoglou, M., Stiffler, D., Stefanakis, Z., Bixler, E.O., and Chrousos, G.P. (2013). Effects of recovery sleep after one work week of mild sleep restriction on interleukin-6 and cortisol secretion and daytime sleepiness and performance. Am. J. Physiol. Endocrinol. Metab. 7, E890– E896.
Biotremology: We Fight for Food Peggy S.M. Hill Professor Emerita, Department of Biological Science, The University of Tulsa, Tulsa, OK 74015, USA Correspondence: [email protected] https://doi.org/10.1016/j.cub.2019.01.061
A new study shines light on an already well-known and mutually beneficial association between ants and the acacia tree. For the first time in this system, plant-borne vibrations introduced by foraging browsers are confirmed as the cue that directs ants to attack the attacker. Most of us know that living things on our planet sometimes form associations with others outside their species, a symbiosis like that of corals in a reef and the algae that give coral its beautiful coloration. We learn this in secondary and college-level textbooks, but also from nature films and online videos, and even from Nemo and the sea anemone. In the USA the term mutualism refers to the type of symbiosis in which both species benefit from the association. This is contrasted with the
other two symbioses: parasitism, where one benefits while the other is harmed (+-), and commensalism, where one benefits and the other is not helped or harmed (+0), as when flying sea birds are incidentally helped to catch fish that have fled to near the surface to escape being eaten by bigger fish. The sea birds benefit from feasting on an aggregation of prey that might otherwise have been inaccessible in deeper water, while the bigger fish are not affected by the sea
Current Biology 29, R200–R223, March 18, 2019 ª 2019 Elsevier Ltd. R209