Clockwork Orangutan: microRNAs, thermoregulatory tradeoffs, and the evolution of brain size.

Abstract

The Expensive Tissue Hypothesis was proposed to account for thermal homeostasis during the evolutionary expansion of brain size in the human lineage and abandoned following publication of a study that found no significant anticorrelations among the body mass-independent residuals of metabolically expensive organs in over 100 mammals, including 23 primates. Re-examination of the same dataset reveals a consistent tradeoff between the liver and brain proportions of a four-organ thermogenic core (kidney, heart, liver and brain), an inherent mechanism of thermoregulation that predates the emergence of permanent homeothermy. The ability of current models of brain size evolution to account for thermal homeostasis is limited by two common assumptions: that organ sizes evolve independently, and that the energy cost of the brain is proportional to the log ratio of brain mass with respect to body mass. Instead, arithmetic ratios provide direct experimental evidence for thermoregulatory constraints on brain size, as do organ cellular metabolic rates (cMRs). These are inferred without log transformation from the parallel adaptive increases in MR/kg and number of microRNA families (mirFam) that have accompanied major shifts in mammalian evolution. The cMR of the liver, the primary organ of gluconeogenesis, varies inversely with that of the brain, the primary consumer of glucose, a phylogenetic plasticity that appears to recapitulate the livers unique developmental plasticity. With mirFam as a proxy for energy reliability, a positive feedback model of relative brain size detected adaptation to a low-energy regime among the smallest primates and, among the largest primates, adaptation to the physiological limit on the rate of heat dissipation.