The evolution of metabolic regulation in animals.

Abstract

Energy metabolism is determined by a suite of regulatory mechanism, and their increasing complexity over evolutionary time provides the key to understanding the emergence of different metabolic phenotypes. Energy metabolism is at the core of biological processes because all organisms must maintain energy balance against thermodynamic gradients. Energy metabolism is regulated by a bewildering array of interacting molecular mechanisms, and much of what is known about metabolic regulation comes from the medical literature. However, ecology and evolutionary research would gain considerably by incorporating regulatory mechanisms more explicitly in research on topics such as the evolution of endothermy, metabolic plasticity, and energy balance. The purpose of this brief review is to summarise the main regulatory pathways of energy metabolism in animals and their evolutionary origins to make these complex interactions more accessible to researchers from a broad range of backgrounds. Some of the principal regulators of energy balance, such as the AMP-stimulated protein kinase, have an ancient prokaryotic origin. Most regulatory pathways (e.g. thyroid hormone, insulin, adipokines), however, are eukaryotic in origin and diversified substantially in metazoans and vertebrates. Diversification in vertebrates is at least partly due to genome duplications early in this lineage. The interaction between regulatory mechanisms permitted an increasingly sophisticated fine-tuning of energy balance and metabolism. Hence, regulatory complexity increased over evolutionary time, and taxa differ in their potential range of metabolic phenotypes. Choice of model organism therefore becomes important, and bacteria or even invertebrates are not good models for more derived vertebrates. Different metabolic phenotypes and their evolution, such as endothermy and metabolic plasticity, should be interpreted against this regulatory background.