Abstract
The paradigm of chronobiology is based almost wholly upon the daily biological clock, or circadian rhythm, which has been the focus of intense molecular, cellular, pharmacological, and behavioral, research. However, the circadian rhythm does not explain biological timings related to fundamental aspects of life history such as rates of tissue/organ/body size development and control of the timing of life stages such as gestation length, age at maturity, and lifespan. This suggests that another biological timing mechanism is at work. Here we focus on a "many days" (multidien) chronobiological period first observed as enigmatic recurring growth lines in developing mammalian tooth enamel that is strongly associate with all adult tissue, organ, and body masses as well as life history attributes such as gestation length, age at maturity, weaning, and lifespan, particularly among the well studied primates. Yet, knowledge of the biological factors regulating the patterning of mammalian life, such as the development of body size and life history structure, does not exist. To identify underlying molecular mechanisms we performed metabolome and genome analyses from blood plasma in domestic pigs. We show that blood plasma metabolites and small non-coding RNA (sncRNA) drawn from 33 domestic pigs over a two-week period strongly oscillate on a 5-day multidien rhythm, as does the pig enamel rhythm. Metabolomics and genomics pathway analyses actually reveal two 5-day rhythms, one related to growth in which biological functions include cell proliferation, apoptosis, and transcription regulation/protein synthesis, and another 5-day rhythm related to degradative pathways that follows three days later. Our results provide experimental confirmation of a 5-day multidien rhythm in the domestic pig linking the periodic growth of enamel with oscillations of the metabolome and genome. This association reveals a new class of chronobiological rhythm and a snapshot of the biological bases that regulate mammalian growth, body size, and life history.
Highlights
Background to life stages and metabolism-mediated developmentThe pace and pattern of life stages is the subject of organismal life history, one of biology's most integrative disciplines
The life histories of mammals are described by a number of characteristics, some of which relate to the timing and duration of life stages
Discriminating between circadian and biological times permits us to ask the question, 'how can biological time be modified to produce the enormous variation in metabolism-mediated development that we observe'? Because timing is fundamental to establishing all aspects of life history, we hypothesize that a periodic rhythm longer than the daily biological clock regulates some aspects of metabolic variability that contribute to variability in body size and the pace and pattern of life
Summary
Background to life stages and metabolism-mediated developmentThe pace and pattern of life stages is the subject of organismal life history, one of biology's most integrative disciplines. While the circadian clock is a key biological mechanism for numerous processes, it has been difficult to link these daily oscillations to the enormous metabolic and life history variation expressed by the entire class of mammals. To address this quandary, we conceptually divide time into two kinds: external time (e.g. daily astronomical variation) that forces circadian time, and biological time (e.g. developmental variation). Because timing is fundamental to establishing all aspects of life history, we hypothesize that a periodic rhythm longer than the daily biological clock regulates some aspects of metabolic variability that contribute to variability in body size and the pace and pattern of life Discriminating between circadian and biological times permits us to ask the question, 'how can biological time be modified to produce the enormous variation in metabolism-mediated development that we observe'? Because timing is fundamental to establishing all aspects of life history, we hypothesize that a periodic rhythm longer than the daily biological clock regulates some aspects of metabolic variability that contribute to variability in body size and the pace and pattern of life
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