Niche Construction: The Neglected Process in Evolution (MPB-37)

Overview

The seemingly innocent observation that the activities of organisms bring about changes in environments is so obvious that it seems an unlikely focus for a new line of thinking about evolution. Yet niche construction -- as this process of organism-driven environmental modification is known -- has hidden complexities. By transforming biotic and abiotic sources of natural selection in external environments, niche construction generates feedback in evolution on a scale hitherto underestimated -- and in a manner that...
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Overview

The seemingly innocent observation that the activities of organisms bring about changes in environments is so obvious that it seems an unlikely focus for a new line of thinking about evolution. Yet niche construction -- as this process of organism-driven environmental modification is known -- has hidden complexities. By transforming biotic and abiotic sources of natural selection in external environments, niche construction generates feedback in evolution on a scale hitherto underestimated -- and in a manner that transforms the evolutionary dynamic. It also plays a critical role in ecology, supporting ecosystem engineering and influencing the flow of energy and nutrients through ecosystems. Despite this, niche construction has been given short shrift in theoretical biology, in part because it cannot be fully understood within the framework of standard evolutionary theory. Wedding evolution and ecology, this book extends evolutionary theory by formally including niche construction and ecological inheritance as additional evolutionary processes. The authors support their historic move with empirical data, theoretical population genetics, and conceptual models. They also describe new research methods capable of testing the theory. They demonstrate how their theory can resolve long-standing problems in ecology, particularly by advancing the sorely needed synthesis of ecology and evolution, and how it offers an evolutionary basis for the human sciences. Already hailed as a pioneering work by some of the world's most influential biologists, this is a rare, potentially field-changing contribution to the biological sciences.
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Editorial Reviews

Times Higher Education Supplement - David Krakauer
In Niche Construction, Odling-Smee et al extend the Darwinian approach to provide a systemic framework for thinking about how environments are modified by organisms and the extent to which these constructed environments influence the evolution of other species.
Ecology - Aaron M. Ellison
Niche construction takes off from standard population genetics theory, but reinvents both the niche and evolutionary theory in ways that require a revolutionary re-thinking of ecological and evolutionary dynamics. . . . A brief review cannot do justice to the excitement that [the authors] generate with their ideas. The relatively simple observation that at least some, if not most organisms modify their environment is shown by [them] to have dramatic consequences for our understanding of evolution by natural selection.
Biology and Philosophy - Samir Okasha
A marvelous achievement. . . . [The authors] present a sustained, rigorous, and highly original argument for the extended evolutionary theory they advocate, that blends theoretical, empirical and philosophical considerations in a most impressive way.
From the Publisher

"In Niche Construction, Odling-Smee et al extend the Darwinian approach to provide a systemic framework for thinking about how environments are modified by organisms and the extent to which these constructed environments influence the evolution of other species."--David Krakauer, Times Higher Education Supplement

"Niche construction takes off from standard population genetics theory, but reinvents both the niche and evolutionary theory in ways that require a revolutionary re-thinking of ecological and evolutionary dynamics. . . . A brief review cannot do justice to the excitement that [the authors] generate with their ideas. The relatively simple observation that at least some, if not most organisms modify their environment is shown by [them] to have dramatic consequences for our understanding of evolution by natural selection."--Aaron M. Ellison, Ecology

"A marvelous achievement. . . . [The authors] present a sustained, rigorous, and highly original argument for the extended evolutionary theory they advocate, that blends theoretical, empirical and philosophical considerations in a most impressive way."--Samir Okasha, Biology and Philosophy

Times Higher Education Supplement
In Niche Construction, Odling-Smee et al extend the Darwinian approach to provide a systemic framework for thinking about how environments are modified by organisms and the extent to which these constructed environments influence the evolution of other species.
— David Krakauer
Ecology
Niche construction takes off from standard population genetics theory, but reinvents both the niche and evolutionary theory in ways that require a revolutionary re-thinking of ecological and evolutionary dynamics. . . . A brief review cannot do justice to the excitement that [the authors] generate with their ideas. The relatively simple observation that at least some, if not most organisms modify their environment is shown by [them] to have dramatic consequences for our understanding of evolution by natural selection.
— Aaron M. Ellison
Biology and Philosophy
A marvelous achievement. . . . [The authors] present a sustained, rigorous, and highly original argument for the extended evolutionary theory they advocate, that blends theoretical, empirical and philosophical considerations in a most impressive way.
— Samir Okasha
Read More Show Less

Product Details

  • ISBN-13: 9780691044385
  • Publisher: Princeton University Press
  • Publication date: 7/2/2003
  • Series: Monographs in Population Biology
  • Pages: 468
  • Product dimensions: 6.10 (w) x 9.30 (h) x 1.00 (d)

Read an Excerpt

Niche Construction

The Neglected Process in Evolution (MPB-37)
By F. John Odling-Smee Kevin N. Laland Marcus W. Feldman

Princeton University Press

Copyright © 2003 Princeton University Press
All right reserved.

ISBN: 978-0-691-04437-8


Chapter One

INTRODUCTION

"To see what is in front of one's nose requires a constant struggle."-George Orwell

Organisms play two roles in evolution. The first consists of carrying genes; organisms survive and reproduce according to chance and natural selection pressures in their environments. This role is the basis for most evolutionary theory, it has been subject to intense qualitative and quantitative investigation, and it is reasonably well understood. However, organisms also interact with environments, take energy and resources from environments, make micro- and macrohabitat choices with respect to environments, construct artifacts, emit detritus and die in environments, and by doing all these things, modify at least some of the natural selection pressures present in their own, and in each other's, local environments. This second role for phenotypes in evolution is not well described or well understood by evolutionary biologists and has not been subject to a great deal of investigation. We call it "niche construction" (Odling-Smee 1988) and it is the subject of this book.

All living creatures, through their metabolism, their activities, and theirchoices, partly create and partly destroy their own niches, on scales ranging from the extremely local to the global. Organisms choose habitats and resources, construct aspects of their environments such as nests, holes, burrows, webs, pupal cases, and a chemical milieu, and frequently choose, protect, and provision nursery environments for their offspring. Niche construction is a strongly intuitive concept. It is far more obvious than natural selection because it is far easier to observe individual organisms doing niche construction than to observe them being affected by natural selection. It is self-evident that all organisms must interact with their environments to stay alive, and equally obvious that, when they do, it is not just organisms that are likely to be affected by the consequences of these interactions, but also environments. That organisms actively contribute toward both the "construction" and "destruction" of their own and each other's niches is scarcely news. So why write a book about it?

The answer is that, when subject to close scrutiny, it becomes clear that niche construction has a number of important, but hitherto neglected implications for evolutionary biology and related disciplines. In fact, in this book we go so far as to argue that niche construction changes our conception of the evolutionary process. Niche construction should be regarded, after natural selection, as a second major participant in evolution. Rather than acting as an "enforcer" of natural selection through the standard physically static elements of, for example, temperature, humidity, or salinity, because of the actions of organisms, the environment will be viewed here as changing and coevolving with the organisms on which it acts selectively.

Using a combination of empirical data, comparative argument, and mathematical modeling we will try to convince the reader of the merits of this new way of thinking about evolution. We will illustrate how niche construction can change the direction, rate, and dynamics of the evolutionary process. Niche construction is a potent evolutionary agent because it introduces feedback into the evolutionary dynamic. Niche construction by organisms significantly modifies the selection pressures acting on them, on their descendants, and on unrelated populations. The later chapters of this book describe how niche construction can be incorporated into empirical and theoretical evolutionary analyses, and how it can be used to generate hypotheses. We will present methods for testing these hypotheses and point to the broad areas of biology and the social sciences to which they are applicable. Our hope is that the niche-construction perspective will prove fruitful by leading to the development of testable new theories and facilitating greater understanding of the evolutionary process.

In this first chapter we introduce the concept of niche construction, and spell out its major consequences with illustrative examples from natural history. We describe four major ramifications of niche construction. Niche construction may (1) in part, control the flow of energy and matter through ecosystems (ecosystem engineering), (2) transform selective environments to generate a form of feedback that may have important evolutionary consequences, (3) create an ecological inheritance of modified selection pressures for descendant populations, and, finally (4) provide a second process capable of contributing to the dynamic adaptive match between organisms and environments (see fig. 1.1). We then consider some of the implications of these consequences for three different bodies of biological theory, namely, evolutionary theory itself, the relationship between evolutionary theory and ecosystem ecology, and the relationship between evolutionary theory and the human sciences.

1.1 THE CONSEQUENCES OF NICHE CONSTRUCTION

1.1.1 Ecosystem Engineering

We begin with an example of a potent niche constructor, the genus of leaf-cutter ants, Atta, as described by the myrmecologists Bert Hölldobler and Edward Wilson (1994). At present, 15 species of leaf-cutter ants are known to science. All of them live in the New World across a geographical range that stretches from the southern states of the United States of America to the south of Argentina. The most salient niche-constructing activity of this genus is "agriculture." Leaf-cutter ants grow fungi on substrates of fresh vegetation that they initially cut and collect from outside their nests and then carry into their nests to form the basis of fungal gardens (fig. 1.2). The fungal crop that the ants grow consists of a fluffy white mold, resembling bread mold, made up of masses of thread-shaped hyphae. The ants' agriculture is so efficient that it not only provides them with an abundant supply of food, but enables individual colonies to reach staggeringly large sizes, with a single colony containing millions of workers. In one extreme case described by Hölldobler and Wilson, a nest of the species Atta sexdens consisted of about a thousand chambers, with the chambers varying in size from that of a closed fist to that of a soccer ball. Three hundred and ninety of its chambers were still in use when it was discovered, and they were filled with both fungal gardens and ants. This particular nest was so huge that the loose soil that had been brought out and piled on the ground by the ants in the course of making their nest occupied over 22 cubic meters and weighed approximately 40,000 kilograms, or 44 tons. Such an example makes it clear that the collective leaf-cutting activities of such large colonies of ants can have enormous impacts on the ants' surrounding environment.

Given such a prodigious capacity for niche construction, it is not surprising that several species of leaf-cutter ants, including Atta cephalotes and Atta sexdens, turn out to be among the worst pests of Central and South America. They destroy billions of dollars worth of agriculturally valuable crops each year. For instance, in Brazil, leaf-cutter ants are especially destructive in eucalyptus and citrus plantations. What is, perhaps, more surprising is that the same ants produce beneficial effects in ecosystems. For example, the ants turn over and aerate large quantities of soil in forests and grasslands, and they also circulate nutrients that are essential to the lives of many other species of organisms with whom they share their ecosystems. Moreover, it has recently been discovered that leaf-cutter ants can help the recovery of rainforests in areas where the primary forest has been destroyed by human farmers and loggers. Here, the ants' activities benefit newly established plants because the soil from their nests is much easier than the surrounding soil for young plant roots to penetrate. Also, the decomposition of the plant material that the ants store in their nests increases the soil's pH, thereby increasing its capacity to retain its nutrients, preventing them from being washed away out of reach of the plants.

Leaf-cutter ants are a good illustration of the first major consequence of niche construction. The activities of organisms can result in significant, consistent, and directed changes in their local environments. Simply by choosing or perturbing their habitats, for example, by repeatedly consuming the same resource, or repeatedly emitting the same detritus, organisms can substantially modify their worlds, and do so in a nonrandom or predictable manner. As a consequence, niche-constructing organisms frequently modify the environments of other organisms too, including organisms in other species. They also affect some of the properties of the ecosystems that they share with other species, in ways that may either harm or benefit other organisms. For instance, as the major herbivores of the neotropics, leaf-cutter ants clearly have an impact on the growth and density of those species of plants that they exploit, as well as on those plants that grow in the improved soil of their nests and those species that rely on the ants to disperse their seeds. Moreover, leaf-cutter ants have glands that secrete substances that kill virtually all bacteria and fungi, except for the single fungus that they cultivate.

While the leaf-cutter ants provide a particularly striking example, there is nothing remarkable about the fact that they have an impact on their local ecology. In chapter 2 of this book we will demonstrate that niche construction is extremely common. Population-community ecologists know a good deal about how organisms can affect each other's environments, both inter- and intraspecifically, and how, by doing so, they can influence such phenomena as the distribution and abundance of organisms, population and community structures, food webs, and trophic dynamics (Begon et al. 1996; DeAngelis 1992; Rosenzweig 1995). Similarly, ecosystem ecologists already have a good understanding of the many ways in which organisms can influence energy and matter flows through ecosystems when they take resources from them, or return detritus to them, and also how their influence can, in turn, affect the structure and function of ecosystems, the resistance and the resilience of ecosystems to perturbations, and the nature of various biogeochemical cycles (O'Neill et al. 1986; Odum 1989; Jones and Lawton 1995; Patten and Jorgensen 1995).

For our purposes, however, a recent insight from a team of ecosystem ecologists, Jones et al. (1994, 1997) and Jones and Lawton (1995), is particularly valuable. Jones et al. describe organisms that choose or perturb their own habitats as "ecosystem engineers," where "ecosystem engineering" is essentially the same as "niche construction." Jones et al. claim that when organisms invest in ecosystem engineering they not only contribute to energy and matter flows and trophic patterns in their ecosystems but in part also control them. They propose that organisms achieve their control via an extra web of connectance in ecosystems, which they call an "engineering web," and which is established by the interactions of diverse species of engineering organisms (Jones et al. 1997). This engineering web operates in conjunction with the familiar material (stoichiometric) and energy (thermodynamic) webs of connectance in ecosystems that are already studied by ecologists (Reiners 1986). Jones et al. also suggest that it is not always necessary for ecosystem engineers to contribute directly to a particular energy or material flow among a set of trophically connected organisms in an ecosystem for them to control the flow (Jones et al. 1997, p. 1952).

We can illustrate these ideas by using two of Jones et al.'s own examples, both taken from the Negev desert in Israel. The first is a case of engineering by microorganisms. In many deserts, including the Negev, the soil is extensively covered by dominant microphytic communities of blue-green algae, cyanobacteria, and fungi. Although these microorganisms are barely visible to the naked eye, they nevertheless have a powerful engineering effect because they secrete polysaccharides that bind the desert's soil and sand together to form a crust that not only protects their own colonies from heat, but also controls erosion, runoff, and site availability for the germination of higher plants in the desert (West 1990; Zaady and Shachak 1994; Jones et al. 1997). After rain, the asphaltlike patches that are created by these microorganisms reduce the absorption of water by about 30%, and this increases the runoff of water, allowing the water to form pools in pits previously dug, for example, by desert porcupines digging for geophytes. Windblown seeds then germinate in these moist pits and give rise to lush oases that may eventually harbor dozens of other species (Alper 1998). Yet all of this ultimately depends on the long reach of the engineering activities of microorganisms.

The second example is provided by three species of snail, Euchondrus spp., that eat endolithic lichens that grow under the surface of limestone rocks in the Negev desert. One consequence of this unusual form of herbivory is that the snails are major agents of rock weathering and also of soil formation in this desert. Their agency, however, is not due to the amount of lichens they consume, which is actually rather little. Instead, it is due to the unexpected fact that these snails have to physically disrupt and ingest the rock substrate in order to consume the lichens. They later excrete the rock material ingested as feces, which they deposit on the soil under the rocks. Shachak et al. (1987) estimated that the annual rate of biological weathering of these rocks by snails is 0.7 to 1.1 metric tons per hectare per year, which is sufficient to affect the whole desert ecosystem (Shachak et al. 1987; Shachak and Jones 1995). By converting rock to soil at this rate, the snails become major agents in soil formation.

So ecosystem control is one major new idea associated with the ecological effects of niche construction. It stems from the capacity of niche-constructing organisms to modify not only their own environments but also the environments of other organisms in the context of shared ecosystems.

1.1.2 The Modification of Selection Pressures

The second consequence of niche construction, and its first evolutionary consequence, derives from these ecological effects. If organisms modify their environments, and if in addition they affect, and possibly in part control, some of the energy and matter flows in their ecosystems, then they are likely to modify some of the natural selection pressures that are present in their own local selective environments, as well as in the selective environments of other organisms. In fact, it is difficult to see how organisms can avoid doing this. Environmental change modifies natural selection pressures (Endler 1986), while organisms are a known source of environmental change in ecology (Jones et al. 1997).

However, in order for niche construction to be a significant evolutionary process, it is not sufficient for niche-constructing organisms to modify one or more natural selection pressures in their local environments temporarily, because whatever selection pressures they do modify must also persist in their modified form for long enough, and with enough local consistency, to be able to have an evolutionary effect. Often this criterion will not be met. Moreover, independent agents in a population's environment may erase or overwhelm the effects of the population's niche construction, thereby ensuring that there is no persistent environmental change caused by the population's activities. For instance, other environmental agents may disperse a population's detritus by dissipating it over time, or, if the agents are detritivores, they may consume the population's detritus, or recycle it, instead of allowing the detritus to accumulate.

There are, however, at least two ways in which this persistence criterion can be satisfied. If, in each generation, each individual repeatedly changes its own ontogenetic environment in the same way, for instance, because each individual inherits genes that express the same niche-constructing phenotypes, then ancestral organisms may modify a source of natural selection by repetitive niche construction. The immediate environmental consequences of this kind of niche construction may be transitory, and may be restricted to single generations only, but if the same environmental change is reimposed sufficiently often and persists for a sufficient number of generations, it may modify the pressures of natural selection in local environments and therefore drive a new evolutionary episode.

(Continues...)



Excerpted from Niche Construction by F. John Odling-Smee Kevin N. Laland Marcus W. Feldman Copyright © 2003 by Princeton University Press . Excerpted by permission.
All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
Excerpts are provided by Dial-A-Book Inc. solely for the personal use of visitors to this web site.

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Table of Contents

List of Figures
List of Tables
Preface
1 Introduction 1
2 The Evidence for Niche Construction 36
3 A Theoretical Investigation of the Evolutionary Consequences of Niche Construction 116
4 General Qualitative Characteristics of Niche Construction 167
5 Niche Construction and Ecology 194
6 Human Niche Construction, Learning, and Cultural Processes 239
7 Testing Niche Construction 1: Empirical Methods and Predictions for Evolutionary Biology 282
8 Testing Niche Construction 2: Empirical Methods, Theory, and Predictions for Ecology 305
9 Testing Niche Construction 3: Empirical Methods and Predictions for the Human Sciences 337
10 Extended Evolutionary Theory 370
App. 1 Model 1a 387
App. 2 Model 1b 404
App. 3 Model 2 408
App. 4 Models 3 and 4 411
App. 5 Model 5 415
Glossary of New Terms 419
Bibliography (indexed) 421
Index 457
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