The evolution of mammalian adipose tissues

Abstract

Anatomical organization, genes and metabolic pathways in white, beige and brown adipose tissues are traced from their invertebrate origins through lower vertebrates to mammals and birds. Invertebrate storage organs and adipose tissues of lower vertebrates are also metabolic regulators. In large turtles, some depots are thermogenic or insulators. Reptilian, avian and mammalian adipocytes sort fatty acids, especially essential polyunsaturates. All mammals have numerous adipose depots, many with site-specific properties including thermoregulation, structural roles or paracrine interactions with contiguous tissues. Paracrine provisioning of lymph nodes with fatty acid sorting optimizes cellular nutrition during fasting or on deficient or imbalanced diets, averts competition with other tissues and utilizes scarce resources efficiently. The mechanisms may be defective in HIV/AIDS and Crohn's disease and some obesity-related diseases. Thermogenesis by shivering and non-shivering mechanisms in muscle occurs in some lower vertebrates and, in birds, is as effective as mammalian brown adipocytes. Facultative thermogenesis emerged gradually in birds and mammals, utilizing genes of reptilian ancestors, including some resembling uncoupling proteins. Mammalian thermogenic tissue evolved from muscle that lost contractile functions and expanded its mitochondria and lipid-storage capacity, thus generating confusing resemblances to white adipocytes. As well as storage and endocrine functions, adipose tissues' capacities for paracrine interactions, fatty acid sorting and thermogenesis supported the evolution of mammalian heterothermy (i.e. diet-induced thermogenesis, torpor and hibernation), lactation and their ability to exploit nutritionally imbalanced diets. These features probably appeared early in mammalian evolution enabling rapid colonization of new habitats, including efficient utilization of poorer quality diets, and metabolic support of lactation that enables fast-growing young to delay maturation of specialised dentitions. The contribution of 'grandmothers' to their descendants' evolutionary fitness drove selection for post-menopausal longevity, aided by larger lower-body superficial depots that protect cardiovascular and metabolic health. Sex differences in human adipose tissue distribution evolved under such sexual selection plus adaptations to heat dissipation. Natural obesity without metabolic impairment found in some arctic mammals evolved by numerous genetic modifications over at least a million years, much longer than human adjustments to modern diet, cooking, heating and clothing.