The first book to address nutrition's complex role in biology
Nutrition has long been considered more the domain of medicine and agriculture than of the biological sciences, yet it touches and shapes all aspects of the natural world. The need for nutrients determines whether wild animals thrive, how populations evolve and decline, and how ecological communities are structured. The Nature of Nutrition is the first book to address nutrition's enormously complex role in biology, both at the level of individual organisms and in their broader ecological interactions.
Stephen Simpson and David Raubenheimer provide a comprehensive theoretical approach to the analysis of nutrition—the Geometric Framework. They show how it can help us to understand the links between nutrition and the biology of individual animals, including the physiological mechanisms that determine the nutritional interactions of the animal with its environment, and the consequences of these interactions in terms of health, immune responses, and lifespan. Simpson and Raubenheimer explain how these effects translate into the collective behavior of groups and societies, and in turn influence food webs and the structure of ecosystems. Then they demonstrate how the Geometric Framework can be used to tackle issues in applied nutrition, such as the problem of optimizing diets for livestock and endangered species, and how it can also help to address the epidemic of human obesity and metabolic disease.
Drawing on a wealth of examples from slime molds to humans, The Nature of Nutrition has important applications in ecology, evolution, and physiology, and offers promising solutions for human health, conservation, and agriculture.
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Stephen J. Simpson is an Australian Research Council Laureate Fellow in the School of Biological Sciences and academic director of the Charles Perkins Centre for the Study of Obesity, Diabetes, and Cardiovascular Disease at the University of Sydney. David Raubenheimer is professor of nutritional ecology at Massey University in New Zealand.
"Debates continue to rage about what diet is best, in part because an underlying theoretical framework for choosing one over another has been lacking. Not so any longer.The Nature of Nutrition demystifies the complexity of nutrition and diet choice and shows why people and other creatures eat the way they do. Along the way, readers learn about the adaptive value of cannibalism, the impact of diet on sex lives, how dietary choices affect entire ecosystems, and so much more."--Daniel Rubenstein, Princeton University
"The Nature of Nutrition is a must-read for anyone interested in the role nutrition plays in the survival of the fittest. Starting with theOrigin of Species, Simpson and Raubenheimer guide us through the nutritional strategies that maintained reproductive health and mating behaviors despite periods of food shortage and danger from predators. The protein leverage hypothesis provides a solid foundation to explain the growing global epidemic of human obesity."--Eric Ravussin, Pennington Biomedical Research Center, Louisiana State University System
"A fascinating and authoritative treatment of nutrition in an ecological and evolutionary framework. Simpson and Raubenheimer's novel perspective crosses disciplines, from the organism to the population to the ecosystem, providing a long-needed unifying framework to what has previously largely been the domain of clinical science."--Simon A. Levin, Princeton University
"This outstanding book provides the first comprehensive theoretical framework for analyzing the roles of nutrition across a huge swath of fields, from ecology and evolution to conservation and human health. The Nature of Nutrition is creative and scholarly yet approachable. I know of no other book like it."--Bernard J. Crespi, Simon Fraser University
"The Nature of Nutrition covers a vast range of issues, from reproduction, immunology, and toxicology to insect migration, population ecology, predator-prey interactions, and ecosystem functioning, as well as applied issues such as conservation biology and human nutritional pathologies. I enjoyed each and every chapter of this excellent book."--Kenneth Wilson, Lancaster University
"Debates continue to rage about what diet is best, in part because an underlying theoretical framework for choosing one over another has been lacking. Not so any longer.The Nature of Nutrition demystifies the complexity of nutrition and diet choice and shows why people and other creatures eat the way they do. Along the way, readers learn about the adaptive value of cannibalism, the impact of diet on sex lives, how dietary choices affect entire ecosystems, and so much more."--Daniel Rubenstein, Princeton University
"The Nature of Nutrition is a must-read for anyone interested in the role nutrition plays in the survival of the fittest. Starting with theOrigin of Species, Simpson and Raubenheimer guide us through the nutritional strategies that maintained reproductive health and mating behaviors despite periods of food shortage and danger from predators. The protein leverage hypothesis provides a solid foundation to explain the growing global epidemic of human obesity."--Eric Ravussin, Pennington Biomedical Research Center, Louisiana State University System
"A fascinating and authoritative treatment of nutrition in an ecological and evolutionary framework. Simpson and Raubenheimer's novel perspective crosses disciplines, from the organism to the population to the ecosystem, providing a long-needed unifying framework to what has previously largely been the domain of clinical science."--Simon A. Levin, Princeton University
"This outstanding book provides the first comprehensive theoretical framework for analyzing the roles of nutrition across a huge swath of fields, from ecology and evolution to conservation and human health. The Nature of Nutrition is creative and scholarly yet approachable. I know of no other book like it."--Bernard J. Crespi, Simon Fraser University
"The Nature of Nutrition covers a vast range of issues, from reproduction, immunology, and toxicology to insect migration, population ecology, predator-prey interactions, and ecosystem functioning, as well as applied issues such as conservation biology and human nutritional pathologies. I enjoyed each and every chapter of this excellent book."--Kenneth Wilson, Lancaster University
Acknowledgments....................................................................................................ixONE Nutrition and Darwin's Entangled Bank..........................................................................11.1 Nutrition Touches and Links All Living Things..................................................................31.2 Nutrition Is Complex...........................................................................................51.3 Dealing with Nutritional Complexity: Enough but Not Too Much...................................................71.4 Charting the Void between Nutritional Detail and Generality: The Geometric Framework...........................10TWO The Geometry of Nutrition......................................................................................112.1 The Geometric Framework: Basic Theory..........................................................................112.2 The Geometric Framework in Practice............................................................................222.3 Conclusions....................................................................................................34THREE Mechanisms of Nutritional Regulation.........................................................................353.1 How to Defend an Intake Target.................................................................................353.2 Postingestive Regulation.......................................................................................483.3 Conclusions....................................................................................................56FOUR Less Food, Less Sex, Live Longer?.............................................................................574.1 How Does Macronutrient Balance Affect Life Span?...............................................................624.2 Less Sex, Live Longer?.........................................................................................664.3 Conclusions....................................................................................................70FIVE Beyond Nutrients..............................................................................................715.1 The Distinction between Nutrients and Toxins...................................................................725.2 Self-medication and Ecological Immunology: The Distinction between Nutrients and Medicines.....................795.3 Toxins and Nutrients Interact..................................................................................845.4 Conclusions....................................................................................................87SIX Moving Targets.................................................................................................886.1 Moving Targets in the Short Term...............................................................................886.2 Moving Targets in Developmental Time...........................................................................916.3 From Parents to Offspring—Epigenetics....................................................................956.4 Evolving Targets...............................................................................................976.5 Evolving Rules of Compromise: Nutrient Specialists and Generalists.............................................996.6 Evolving Postingestive Responses...............................................................................1056.7 Conclusions....................................................................................................106SEVEN From Individuals to Populations and Societies................................................................1087.1 Cannibal Mormon Crickets.......................................................................................1097.2 Locusts Are Cannibals Too......................................................................................1137.3 Communal Nutrition in Ants.....................................................................................1147.4 The Blob.......................................................................................................1177.5 Conclusions....................................................................................................119EIGHT How Does Nutrition Structure Ecosystems?.....................................................................1208.1 From Individual Fitness to Population Growth Rates.............................................................1218.2 Interactions among Organisms and the Environment...............................................................1228.3 Do Predators Regulate Nutrient Intake?.........................................................................1248.4 The Nutritional Geometry of Food Webs..........................................................................1308.5 The Nutritional Niche..........................................................................................1388.6 Agent-Based Modeling of Nutritional Interactions: From Individuals to Ecosystems...............................1448.7 Conclusions....................................................................................................145NINE Applied Nutrition.............................................................................................1479.1 Domestication..................................................................................................1479.2 Wildlife Conservation..........................................................................................1579.3 Conclusions....................................................................................................165TEN The Geometry of Human Nutrition................................................................................16710.1 The Modern Human Nutritional Dilemma..........................................................................16710.2 Do Humans Regulate to an Intake Target?.......................................................................17010.3 What Is the Human Rule of Compromise?.........................................................................17510.4 What Are the Implications of Protein Leverage?................................................................18210.5 How Do Humans Deal with Nutrient Excesses?....................................................................19110.6 Conclusions...................................................................................................191ELEVEN Perspectives................................................................................................19411.1 Expanding GF into Further Dimensions of Nutrition.............................................................19411.2 GF and "Omics"................................................................................................19511.3 Nutritional Epigenetics and Early-Life Prevention of Metabolic Disease........................................19611.4 Human Obesity.................................................................................................19611.5 Nutritional Immunology........................................................................................19711.6 Modeling Nutritional Interactions: From Individuals to Ecosystems.............................................19811.7 Conclusions...................................................................................................199References.........................................................................................................201Index..............................................................................................................229
Charles Darwin (1859) famously ended his revolutionary book The Origin of Species with a paragraph that opened:
It is interesting to contemplate an entangled bank, clothed with many plants of many kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent on each other in so complex a manner, have all been produced by laws acting around us.
Darwin demonstrated in his book that a few biological facts—what he refers to as "laws"—combine to provide an elegantly simple natural mechanism that can explain the origin of the diverse and elaborately constructed plants and animals in his "entangled bank." The facts are reproduction with inheritance, variability, and competition for resources; the mechanism is natural selection.
The theory of natural selection provided a framework that encompassed all of biology. But Darwin was well aware that within this framework there were daunting webs of entangled complexity that remained to be unraveled. The "elaborately constructed" organisms—the meshwork of interactions between molecules, organelles, tissues, and organs that furnished Darwin with clear evidence of adaptation to the environment—remained poorly understood, as did the ecological interactions through which these organisms were "dependent on each other in so complex a manner."
Much of biology over the past 150 years has been focused on unraveling this complexity. Armed with progressively more powerful technologies, and sophisticated numerical and conceptual tools, functional biologists, ecologists, and applied biologists have worked away at the task, sometimes with incremental gains, sometimes with transformational advances. Darwin would be astounded by the progress that has been made.
But an important opportunity has been neglected: the potential offered by following the connections provided by nutrition. Nutrition touches, links, and shapes all aspects of the biological world. It builds the components of organisms, and fuels the dynamic interactions between these components; it determines whether or not wild animals thrive, how their populations grow, decline, and evolve, and how assemblages of interacting species (ecological communities) and ecosystems are structured. Nutrition also drives the affairs of humans, from individuals to global geopolitics. Food security and the burden of famine and disease from undernutrition have been pervasive in history, and recently overnutrition has emerged as a major cause of preventable death and disease. Climate change, population growth, urbanization, environmental degradation, and species extinctions all are in one way or another linked to the need for nutrients. In short, nutrients are the interconnecting threads in the web of life.
And yet the science of nutrition remains fragmented. Because of its direct importance to human health and food-animal production, nutrition has traditionally been considered the domain of the medical and agricultural sciences. Research in these areas has produced a tremendously detailed account of the nutritional biology of a few species. By contrast, with some exceptions, nutrition in the ecological sciences has tended to adopt simpler, more general approaches that are applicable across the diversity of animals. Foraging might, for example, be considered a process of acquiring energy or minimizing time exposed to predators, rather than a complex balancing act of obtaining enough—but not too much—of the many nutrients that are needed for sustaining health and reproduction. The advantage of this simplified approach is that it has supported the development of powerful general frameworks for biological processes, unhindered by the staggering nutritional complexity that has been uncovered in the more applied nutritional sciences.
We believe, however, that considerable potential for unraveling Darwin's entangled bank lies unutilized in the void between the blinding detail of nutrition in the applied sciences and the conveniently simplistic nutritional frameworks of the ecological sciences. Our aim in this book is to present an approach that can help to realize this potential, by systematically introducing nutritional complexity into the ecological sciences, while providing a scaffold for extracting generalities from the mass of detail in applied nutrition. We hope that this approach, called the "Geometric Framework," will help to disentangle the rich and complex network of interconnections that bind the web of life, and to elucidate how mismanagement in one area can lead to intractable tangles elsewhere.
In this chapter we briefly expand on three important themes that form the backdrop to our story: nutrition touches and links all living things; nutrition is complex; and there have been benefits both from the highly specific and detailed approach of applied nutritional sciences and the simplified, general approaches adopted in the ecological sciences. In the rest of the book we show how simple geometry can be used to explore the middle ground, by systematically introducing enough complexity to help navigate the extensive network from detailed biological mechanisms to large-scale ecosystem processes.
1.1 Nutrition Touches and Links all Living Things
At the most conspicuous level, nutrition is a primary factor defining the geographic distribution and temporal pattern of activity for many animals (Raubenheimer 2010). It is true that the geographical and temporal patterns of animals are also governed by factors other than nutrition, such as the location of mates and the activities of predators. But mates, too, need to feed, and the problem with predators is that they aim to do just that.
Indeed, in many animal systems the spatial and temporal patterns of reproduction are tightly geared toward resource availability. Extreme examples include the movements of caribou, wildebeest, and locusts, where hordes of animals migrate over vast distances to coordinate breeding with food availability. In other cases, such as the critically endangered New Zealand kakapo parrot, breeding occurs on average once every two to five years, when the fruits needed for rearing chicks are superabundant (Elliott et al. 2001). In yet other animals, breeding success has been linked not to food availability but specifically to the nutritional composition of prey. For example, recruitment of kittiwake gulls is higher when lipid-rich fish are available compared with lipid-poor species. Experiments suggest that a lipid-poor diet does not support normal brain development, resulting in cognitively impaired chicks (Kitaysky et al. 2006).
The role of nutrition in brain development has also been linked to mating success. It has been suggested, for example, that complex song learning has evolved in birds as a means of demonstrating to potential mates a high degree of cognitive competence—showing off, as it were. Nowicki and colleagues (1998) have argued that the ability to learn complex songs is dependent on good brain development, which in turn is influenced by nutrition. A complex song repertoire can thus provide an indication to females that a male has been well nourished in development, and therefore that she is mating into a family that is competent at foraging. Alternatively, a complex song repertoire could indicate that the male has genes that direct good development regardless of whether there have been nutritional perturbations during development. Either way, nutrition is central.
And this is true not only for birdsong but also for other animal signals. Carotenoids, for example, are color pigments widely used in visual signals by birds. Since birds cannot synthesize these compounds but must obtain them from the foods they eat, a good supply of carotenoids is dependent on their foraging ability. If carotenoids are limiting in the environment, then by selecting a bright male a female can ensure that she mates with a competent forager that will be able to provide for her offspring. Furthermore, carotenoids are used not only as signals but also for a range of physiological functions including immunoregulation. Bright coloration might therefore indicate to a potential mate not only good foraging ability but also good health. This is believed to underlie the evolution of bright flanges in the mouths of nestlings of some species of birds. By preferentially feeding the chicks with brighter mouths, the parents can ensure that they direct the profits of their foraging efforts toward healthy offspring (Dugas 2010). Carotenoids are important not only in signaling and health but also in vision (Toomey and McGraw 2009). In birds, for example, carotenoids accumulate in the oil droplets of retinal cones and act as selective filters that enhance color vision. They also protect the retina, by absorbing harmful ultraviolet radiation.
The UV-protective function of carotenoids can be an important determinant of the geographical distribution of animals. Sommaruga (2010), for example, has shown that the concentration of carotenoids in crustacean zooplankton species is strongly related to the extent to which their lake habitats expose them to UV radiation—plankton in clear, shallow, high-altitude lakes have higher carotenoid concentrations than those in deeper, more turbid lakes. Another class of diet-derived photoprotective compounds that has been related to the degree of UV exposure in plankton is the mycosporine-like amino acids (MAA). The balance of carotenoids to MAAs varies widely in zooplankton populations, and many interesting studies have addressed the question of what determines this balance (Hylander et al. 2009). One primary determinant is availability: MAAs occur only in some of the algal foods of zooplankton, and the availability of these varies among lakes; carotenoids, by contrast, are more widely available. A second important determinant has to do not with the trophic level below the zooplankton but that above—MAAs are colorless and therefore, unlike carotenoids, do not increase the conspicuousness of plankton to predators. Consequently, zooplankton exposed to a high risk of predation by visual predators like fish tend to adopt MAAs as the chosen sunscreen. If MAAs are not available, however, the zooplankton need to resolve the dilemma of whether to protect against UV damage but suffer increased predation, or avoid predation and suffer the ravages of sunburn. In experiments where copepods were exposed to a combination of predation, high UV, and low MAA supply, they opted for the sunburn over increased predation (Hylander et al. 2009).
Other experiments have demonstrated that exposure to predation can alter the balance of macronutrients required by animals. Hawlena and Schmitz (2010) compared the balance of protein to carbohydrate selected by grasshoppers in the presence and absence of spider predators. Their results showed that the presence of spiders caused the grasshoppers to select a diet higher in carbohydrate relative to protein, as opposed to when spiders were absent. A separate experiment suggested a reason for this: the stress caused by the presence of the predators resulted in a 32% increase in the metabolic rate of the grasshoppers, and the shift in the selected diet was evidently a compensatory response to meet these added energy costs. Other experiments have shown that locusts also compensate in this way to meet the energetic costs of flight, and rats do so to meet the costs of thermoregulation in cold environments (Raubenheimer and Simpson 1997). Similar nutrient-specific responses have been observed in predatory beetles as they emerge from winter diapause: they initially select a diet high in fat relative to protein, and as the body fat that was depleted during the previous winter is replenished, they increase their intake of protein to meet reproductive demands (Raubenheimer et al. 2007).
We have tried to illustrate in the preceding paragraphs how pervasive nutrition is: start with the habitat selection and activity patterns of animals, and you can seamlessly transition via a network of nutritional interconnections to brain development, birdsong, animal coloration, parental care, retinal function, natural sunscreens, diapause, flight, stress responses, thermoregulation, and an illustration of how nutrition can mediate complex relationships between food availability, predation risk, and threats from solar radiation. We could continue indefinitely, expanding the range of nutrients, contexts, and problems. However, the chapters that follow provide many further examples illustrating just how pervasive nutrition is, and elaborate on some of those introduced above. For now we will leave this topic and turn to the related issue of the complexity of nutrition.
1.2 Nutrition Is Complex
For some animals, the challenges of feeding appear relatively straightforward. Many species of butterflies, for example, forage only for nectar, which consists largely of energy-rich sugars and water. For them, nutrition appears to be a simple process of matching carbohydrate acquisition to carbohydrate requirements. Most animals, by contrast, need to forage for more complex resources, comprising also amino acids, vitamins, minerals, and a range of other food components. But even here, foraging need not be a complex task, if the available foods contain all these nutrients in the required balance. It is widely believed that this is the case for predators. These animals are considered to feed on high-quality foods that are relatively similar to the predator and to one another in composition (i.e., the bodies of other animals), and consequently the principal challenge they face is to capture enough of these high-quality foods to satisfy their needs (Stephens and Krebs 1986).
On closer inspection, however, even these apparently simple cases are deceptively complex. Butterflies, for example, are not physiologically exempt from the requirements for amino acids, vitamins, and the full range of nutrients that other animals need to survive and reproduce. Rather, in those species that as adults feed only on nectar, the task of acquiring the broader range of nutrients falls to the larval (caterpillar) stage—the adult draws on stores accumulated in its youth. The caterpillars therefore face the doubly complex foraging task of ensuring that they acquire enough of the various nutrients to satisfy their immediate needs as well as their future needs, both as adults and in the nonfeeding pupal phase, during which larval tissues are reconstructed into the adult body form.
Likewise, it is also almost certainly the case that the foraging challenges of carnivores are more complex than meets the eye. First, accumulating evidence suggests that the body composition of prey animals can be highly variable (Fagan et al. 2002; Raubenheimer et al. 2007; Spitz et al. 2010; Raubenheimer 2011). Second, in common with other animals, the nutrient needs of predators are not fixed, but change—for example, as they grow, and with different levels of activity, with changes in their health status, and so forth. It is therefore unlikely that any one food will provide the right balance of nutrients throughout the life of the animal, and most predators will need to actively balance their nutrient gain by selecting foods appropriately and/or physiologically regulating the relative efficiency of nutrient retention. Third, it has been demonstrated in laboratory experiments that both vertebrate (Sánchez-Vázquez et al. 1999; Mayntz et al. 2009; Hewson-Hughes et al. 2011) and invertebrate predators (Mayntz et al. 2005) feed selectively in relation to the nutrient composition of foods, suggesting that they are adapted to dealing with variation in the match between nutrient needs and food compositions. The predatory ground beetle mentioned in the previous section illustrates all these points: its nutrient requirements change during the time it emerges from diapause and approaches reproductive maturity; its pattern of nutrient selection tracks these requirements; and its body composition (and hence its suitability as food for other predators) changes markedly during this period (Raubenheimer et al. 2007).
(Continues...)
Excerpted from The Nature of Nutritionby Stephen J. Simpson David Raubenheimer Copyright © 2012 by Princeton University Press. Excerpted by permission of PRINCETON UNIVERSITY PRESS. All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
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