Books and Arts

Nature 425, 769-770 (23 October 2003) | doi:10.1038/425769a

Changing the world

Laurent Keller1

BOOK REVIEWEDNiche Construction: The Neglected Process in Evolution

byF. John Odling-Smee, , Kevin N. Laland & & Marcus W. Feldman


Princeton University Press: 2003. 486 pp. $75, £49.95 (hbk); $39.50, £26.95 (pbk)

Changing the world

AL GRANT

"Niche construction changes our conception of the evolutionary process ... and should be regarded, after natural selection, as a second major participant in evolution." So argue the authors of this book as early as page 2. But what exactly is niche construction? And if it's really so important, how could evolutionary biologists have neglected it for so long?

The concept of niche construction is relatively simple. All living creatures, through both their metabolism and their behaviour, actively change and control the world in which they live. Organisms choose habitats and resources; they construct nests, holes, burrows, webs or pupal cases; and they modify the chemical environment in which they live. These alterations, which occur at scales ranging from the extremely local to the global, inevitably modify some of the selection pressures acting on the organisms. And it is precisely this — the effects of an organism on its own environment — that the authors believe to be the important component that has been neglected by the conventional theory of evolution.

The concept that organisms bring about important changes in their environment that may in turn affect their fitness is not completely new, however. Charles Darwin had already made several potent observations to this effect. For example, in On the Origin of Species he states: "When a species, owing to highly favourable circumstances, increases inordinately in numbers in a small tract, epidemics — at least this seems generally to occur with our game animals — often ensue: and here we have a limiting check independent of the struggle for life." This observation is strongly reminiscent of one in Niche Construction in which the authors discuss how large-scale human aggregation resulting from the construction of villages, towns and cities may create new health hazards such as the spread of epidemics.

In the 1980s, several scientists pointed out that organisms not only adapt to their environment but construct it as well. In The Extended Phenotype (Freeman, 1982), Richard Dawkins argues that genes can express themselves outside the bodies of the organisms that carry them, an example being a beaver's dam. Richard Lewontin, in his contribution to Evolution from Molecules to Men (Cambridge University Press, 1983), also realized that the histories of organisms and the environment are a function of each other. He therefore suggested that what is actually happening in nature could be represented by a pair of coupled differential equations.

Niche Construction goes one step further by providing an exhaustive list of the possible effects of organisms on their environment, from the alteration of non-living environments to various sorts of maternal effects induced by differences in the levels of yolk, hormones and messenger RNA in the cytoplasm. In humans, cultural processes constitute an additional kind of non-genetic information that is transmitted from one generation to the next. The authors correctly argue that niche construction may result in evolutionary feedback, with the evolutionary trajectories of organisms being influenced by the changes that they induce on their environment. Feedback also occurs across generations, with individuals being influenced by the environmental modifications provoked by their ancestors.

To make their point, the authors list numerous examples. One of the most striking is the evolution of lactose tolerance. The domestication of cattle brought milk and dairy products into the diet of some human populations for enough generations to promote genes that confer greater lactose tolerance. Another example of a culturally induced genetic signature relates to the influence of agricultural niche construction on natural selection. The Kwa-speaking yam cultivators of West Africa made clearings in tropical rainforests, increasing the amount of standing water. This provided superior breeding grounds for malaria-carrying mosquitoes, which in turn increased the prevalence of malaria. At the same time, the frequency of the haemoglobin allele responsible for sickle-cell anaemia increased, as people who have one copy of this allele have some resistance to malaria. These examples demonstrate how cultural processes are not just a product of human genetic evolution but also a cause of it.

So does this mean that we need a new, extended theory of evolution as advocated by Niche Construction? I believe that the answer is no. First of all, the examples of niche construction given in the book can be explained by conventional evolutionary theory once all of the relevant environmental factors are taken into account. Several elegant models — including some developed by the authors themselves — have already been proposed to deal with feedback effects between organisms and their environment. At the same time, it is not possible to develop an extended theory of evolution that can encompass all of the different types of niche-construction effects. Interactions between organisms and their environment are, by their very nature, complex and result in an intricate web of interacting effects. No heuristic theory could integrate all of these effects without becoming intractable, so we need to devise specific models for each situation. Indeed, evolutionary biologists are already doing exactly this.

To summarize, Niche Construction does an excellent job of detailing the many ways in which organisms modify their environment and hence the selective forces acting on them. But it is unfortunate that the authors attempt to oversell the significance of niche construction. By advocating a grand, extended evolutionary theory, they distract readers from the more important message of the book, which is that the influence of organisms on their environment can have far-reaching consequences. Indeed, humans are currently working hard at building a vivid example of this. By allowing the massive-scale niche destruction that is currently under way, we are not only compromising the environment, but also affecting the prospects and evolutionary trajectories of our children and many later generations.

  1. Laurent Keller is in the Department of Ecology and Evolution, Biology Building, University of Lausanne, 1015 Lausanne, Switzerland.