Activity patterns in mammals: Circadian dominance challenged

ESSAY Activity patterns in mammals: Circadian dominance challenged David G. Hazlerigg ID1*, Nicholas J. C. Tyler ID2 1 Department of Arctic and Marine Biology, UiT The Arctic University of Norway, Tromsø, Norway, 2 Centre for Saami Studies, UiT The Arctic University of Norway, Tromsø, Norway * Abstract a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS The evidence that diel patterns of physiology and behaviour in mammals are governed by circadian ‘clocks’ is based almost entirely on studies of nocturnal rodents. The emergent circadian paradigm, however, neglects the roles of energy metabolism and alimentary function (feeding and digestion) as determinants of activity pattern. The temporal control of activity varies widely across taxa, and ungulates, microtine rodents, and insectivores provide examples in which circadian timekeeping is vestigial. The nocturnal rodent/human paradigm of circadian organisation is unhelpful when considering the broader manifestation of activity patterns in mammals. Citation: Hazlerigg DG, Tyler NJC (2019) Activity patterns in mammals: Circadian dominance challenged. PLoS Biol 17(7): e3000360. https://doi. org/10.1371/journal.pbio.3000360 Academic Editor: Achim Kramer, Charité Universitätsmedizin Berlin, GERMANY Published: July 15, 2019 Copyright: © 2019 Hazlerigg, Tyler. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: DGH was supported by HFSP program grant RGP0030/2015-C301 "Evolution of seasonal timers". The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Abbreviations: LBM, live body mass; LC, light-dark cycle; NLC, no-light cycle; SCN, suprachiasmatic nucleus; Tb, body temperature; Tlc, lower critical temperature. Provenance: Not commissioned; externally peer reviewed It is widely held that daily patterns of physiology and behaviour in mammals are governed by the cell-autonomous rhythms of gene transcription that constitute circadian ‘clocks’ [1]. Circadian clocks have been identified and characterised in species ranging from cyanobacteria to humans, and circadian organisation is generally considered a ubiquitous controlling feature [2–5]. The empirical basis for this view, however, is surprisingly weak. Knowledge of circadian mechanisms stems from studies in model organisms in which the phenotype is prominent and, in mammals, is based almost entirely on studies in rats, mice, and hamsters. This is no coincidence: these small nocturnal rodents are cheap to maintain, perform well in the laboratory, and above all, display strong circadian organisation. Had this not been the case, they would not have been studied: they were selected as models of circadian function, not of their taxa. The ascendancy of the circadian model has led to uncritical use of the term ‘circadian’. Identification of circadian organisation (sensu stricto) requires evidence of persistence—i.e., the demonstration that rhythms are expressed in the absence of external synchronising input (the so-called zeitgeber). Such evidence is normally sought by observing organisms such as humans and mice under constant conditions―most often continuous darkness or dim red light. The term ‘circadian’ is nevertheless frequently ascribed in scientific literature to rhythms recorded under daily cycles of light intensity. Such usage without evidence of endogenous drive renders the term ‘circadian’ synonymous with ‘24 h’ or ‘diel’ and therefore redundant. PLOS Biology | https://doi.org/10.1371/journal.pbio.3000360 July 15, 2019 1 / 10 Fig 1 shows examples of two species from distinct mammalian taxa (common vole [Microtus arvalis] and reindeer/caribou [Rangifer tarandus L.], hereafter Rangifer) in which circadian organisation is not evident. Occurrence of noncircadian temporal organisation like this should make us wonder what circumstances have promoted circadian dominance in some species— notably, those upon which the canon is founded. Maintenance of thermal balance is a major determinant of temporal activity patterns in small mammals [10], for which, moreover, the world is generally a cold place. Thus, although hyperthermia may be a problem in some environments (e.g., hot deserts), the mean surface temperature of the earth (14˚C [11]) is substantially lower than the lower critical temperature (Tlc) of small mammals (<100 g; median Tlc = 29˚C, range = 20 to 36, n = 218 species [12,13], Fig 2). Such creatures are obliged to sustain a high metabolic rate simply to maintain body Fig 1. Circadian organisation is not ubiquitous in mammals. Activity patterning in (from the top) humans, mice (Mus musculus), voles (M. arvalis), and reindeer (R. tarandus) under 24-h LCs and NLCs. All four species display pronounced 24-h rhythms of activity under LC. These rhythms persist under NLC in humans and mice but not in voles and reindeer. Data for humans are from bunker experiments in which subjects were initially exposed to changes in light intensity synchronised to the solar day (LC) and then allowed to free-run with only self-imposed changes in light level (NLC [6]). For mice and voles, experimental light and dark phases are represented by horizontal white and brown bars, respectively. For the reindeer, free-living in their natural environment, natural photoperiod (onset and offset of civil twilight) is indicated by vertical yellow lines on the first day of each actogram, and the NLC regime was the polar night at 78˚ north latitude. Data for one individual of each species under each light regime are presented as double-plotted actograms. Black bars represent activity. LC, light–dark cycle; NLC, no-light cycle. Redrawn from [6–9]. https://doi.org/10.1371/journal.pbio.3000360.g001 PLOS Biology | https://doi.org/10.1371/journal.pbio.3000360 July 15, 2019 2 / 10 Fig 2. Relationship between Tlc (˚C) and body mass (g) in mammals. The Tlc is defined as the ambient temperature below which the rate of metabolic heat production must be increased in order to maintain homeothermy. Of all species with Tlc above the global mean surface temperature (14˚C, horizontal dashed line; [11]), humans (Tlc range from 23 to 33˚C; [16,17]) are the most massive, and of all species with a body mass above 50 kg (vertical dashed line), humans have the highest Tlc. For clarity, the figure includes only data for a limited number of taxa (humans, Carnivora, nonhuman primates, Rodentia, ruminants). However, the shape of the relationship between body mass and Tlc does not change when data for other groups are included (Chiroptera, Cingulata, Dasyuromorphia, Diprotodontia, Erinaceomorpha, Eulipotyphla, Hyracoidea, Lagomorpha, Macroscelidea, Monotremata, (...truncated)