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Symonds - Adipose Tissue Biology

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Symonds Adipose Tissue Biology
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Springer Science+Business Media LLC 2017
Michael E. Symonds (ed.) Adipose Tissue Biology 10.1007/978-3-319-52031-5_1
1. The Evolution of Mammalian Adipose Tissues
Caroline M. Pond 1, 2
(1)
School of Life, Health & Chemical Sciences, The Open University, Milton Keynes, MK7 6AA, UK
(2)
Department of Zoology, Oxford University, South Parks Road, Oxford, OX1 3PS, UK
Caroline M. Pond
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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 Crohns 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.
Keywords
Comparative Reptiles Mammals Birds Primates Apes Bears Paracrine interactions Immune system Fatty acids Perinodal Crohns disease Colitis Lipid-soluble toxins Hibernation Diet-induced thermogenesis Herbivory Lactation Thrifty genes Sex differences Cold adaptation
1.1 Introduction
For many centuries, comparative biology and medicine advanced in parallel, with many practitioners making important and mutually beneficial contributions to both fields. Increasing specialization in the twentieth century forced them apart until the rise of molecular phylogeny, medical genomics and developmental biology in the 1990s reunited the estranged partners. Adipose tissues have been one of the most spectacular beneficiaries of this rapprochement: comparative and medical biologists now recognise that their findings are as mutually supportive to each others progress as they have even been. This chapter is a three-way synthesis of comparative concepts from wild animals in natural systems, experimental data from laboratory animals & ex vivo cultures and human studies to elucidate the normal functions and pathologies of adipose tissues.
Although research involving adipose tissues has expanded enormously during the past 50 years (Rosen and Spiegelman ), evolutionary and comparative studies lagged behind metabolism, endocrinology and human epidemiology. Both white (WAT) and brown (BAT) adipose tissues have been largely omitted from genetic and developmental investigations into the origins and evolution of tissues and cell types that complement the long-established discipline of comparative anatomy, functionality and adaptation because they appear too variable, too closely linked to diet and body condition to reveal any general principles determining their site-specific properties and anatomical distribution or phylogenetic relationships to lean tissues.
Interest in its origins and evolution was stimulated by recognition of WATs endocrine and paracrine relationships, its role in metabolic regulation and its value as a source of stem cells and in reconstructive surgery as well as lipid storage and recently accelerated by the study of the uniquely mammalian tissues BAT and beige or brite adipocytes (Cohen and Spiegelman ).
1.1.1 Comparative Perspectives on Obesity and Diabetes
Obesity and adipose tissues, almost synonymous in the mid-twentieth century, drifted apart as the focus of the former shifted to appetite control and inheritance and of the latter to adipokines (Dodson et al. ).
Of several recent attempts to account for the evolution of obesity in humans, some hardly mention current understanding of the organisation and basic properties of adipose tissues (Power and Schulkin ).
Obesity is unusual among human diseases in that very similar conditions are integral and essential components of the habits and life history of certain wild animals. Natural obesity, like pathological obesity, arises from overeating, periods in which animals become hyperphagic, in some cases aided by sedentary habits. But in wild animals, obesity is always transient and controlled: hyperphagia and fat deposition are followed by periods of anorexia and/or intensive exercise, leading to weight loss (Pond ). Adaptive obesity is never a direct cause of diabetes, cardiovascular disease or reproductive dysfunction. The study of natural obesity can reveal much about the ideal structure, composition and anatomical distribution of adipose tissue, the neural and endocrine control of blood composition, appetite and energy expenditure and about the causal relationships between high levels of stored lipid and the adverse metabolic changes that are so frequently associated with obesity in humans.
The origins and incidence of Type 2 diabetes have been explored in many dimensions from metabolism, molecular signalling and immunity to human evolution, ecology and social behaviour (Watve ), though not yet with gross anatomy and the contributions of different organs and tissues. The evolution of adipose tissues, their gross anatomy and relations with other tissues, and, at the microscopic level, adipocytes and the many other cell types they incorporate, have until recently received little attention.
Comparative physiology and genomics during the past 20 years have demonstrated remarkable similarities in the relationships between diet, metabolic control, energy storage and key life history parameters including longevity and fecundity (Fontana et al. ). Therefore, it is appropriate to begin with an evolutionary and comparative perspective on the structure and functions of adipose tissues.
1.2 Storage Tissues
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