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Niche Construction and Their Implications for Ecology (Ecosystem Engineering͞adaptation)

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Niche Construction and Their Implications for Ecology (Ecosystem Engineering͞adaptation) Proc. Natl. Acad. Sci. USA Vol. 96, pp. 10242–10247, August 1999 Evolution Evolutionary consequences of niche construction and their implications for ecology (ecosystem engineering͞adaptation) K. N. LALAND†‡,F.J.ODLING-SMEE§, AND M. W. FELDMAN¶ †Sub-department of Animal Behavior, University of Cambridge, Madingley, Cambridge CB3 8AA, United Kingdom; §Institute of Biological Anthropology, Oxford University, 58 Banbury Road, Oxford OX2 6QS, United Kingdom; and ¶Department of Biological Sciences, Herrin Hall, Stanford University, Stanford, CA, 94305-5020 Communicated by Paul R. Ehrlich, Stanford University, Stanford, CA, June 21, 1999 (received for review December 21, 1998) ABSTRACT Organisms regularly modify local resource ment (11, 12). The construction of artifacts is equally common distributions, influencing both their ecosystems and the evo- among vertebrates. Many mammals (including badgers, go- lution of traits whose fitness depends on such alterable phers, ground squirrels, hedgehogs, marmots, moles, mole sources of natural selection in environments. We call these rats, opossum, prairie dogs, rabbits, and rats) construct burrow processes niche construction. We explore the evolutionary systems, some with underground passages, interconnected consequences of niche construction using a two-locus popu- chambers, and multiple entrances (13). Here, too, there is lation genetic model, which extends earlier analyses by allow- evidence that burrow defense, maintenance, and regulation ing resource distributions to be influenced both by niche behaviors have evolved in response to selection pressures that construction and by independent processes of renewal and were initiated by the construction of the burrow (11, 13). depletion. The analysis confirms that niche construction can Most cases of niche construction, however, do not involve be a potent evolutionary agent by generating selection that the building of artifacts but merely the selection or modifica- leads to the fixation of otherwise deleterious alleles, support- tion of habitats. For example, as a result of the accumulated ing stable polymorphisms where none are expected, eliminat- effects of past generations of earthworm niche construction, ing what would otherwise be stable polymorphisms, and present generations of earthworms inhabit radically altered generating unusual evolutionary dynamics. Even small environments where they are exposed to modified selection amounts of niche construction, or niche construction that only pressures (14, 15). Previously, we described this legacy of weakly affects resource dynamics, can significantly alter both modified selection pressures as an ‘‘ecological inheritance.’’ ecological and evolutionary patterns. Nor is niche construction confined to animals. Plants change the chemical nature, the pattern of nutrient cycling, the There is increasing recognition that all organisms modify their temperature, the humidity, the fertility, the acidity, and the environments (1), a process that we call ‘‘niche construction’’ salinity of their soils and the patterns of light and shade in their (2) but is elsewhere described as ‘‘ecosystem engineering’’ (3). habitats (16–19). For instance, pine and chaparral species Such modifications can have profound effects on the distribu- increase the likelihood of forest fires by accumulating oils or tion and abundance of organisms, the influence of keystone litter, with the probable evolutionary consequence of having species, the control of energy and material flows, residence evolved a resistance to fire and in some species a dependency and return times, ecosystem resilience, and specific trophic on it (20–22). relationships (3–6). The consequences of environment modi- We have explored the dynamics of the joint evolution of fication by organisms, however, are not restricted to ecology, environment-altering, niche-constructing traits in organisms and organisms can affect both their own and each other’s and other traits whose fitness depends on feedback from evolution by modifying sources of natural selection in their natural selection in environments that can be altered by niche environments (2, 7). We have argued that niche construction construction (9). Our previous analysis used a two-locus is responsible for hitherto-neglected forms of feedback in population-genetics model, with alleles at one locus influenc- evolution, whereby legacies of ancestrally modified natural ing the population’s niche construction by affecting the selection pressures affect the subsequent evolution of later amount of a key resource in the environment and with the generations of organisms (7–9). amount of the resource influencing the contribution to fitness There are numerous examples of organisms choosing or of genotypes at a second locus. Our analysis suggested that the changing their habitats or constructing artifacts, leading to an changes that organisms bring about in their own selective evolutionary, as well as an ecological, response (see refs. 2, 3, environments can be an important source of modified natural- and 7–9). For instance, orb-web spiders construct webs, which selection pressures and can generate some unusual evolution- have led to the subsequent evolution of camouflage, defense, ary outcomes. For example, niche construction can cause and communication behavior on the web (10). Similarly, ants, evolutionary inertia and momentum, it can lead to the fixation bees, wasps, and termites construct nests that are themselves of otherwise deleterious alleles, it can support stable polymor- the source of selection for many nest regulatory, maintenance, phisms where none are expected, and it can eliminate what and defense behavior patterns. For example, many ant and would otherwise be stable polymorphisms. termite species regulate temperature by plugging nest en- Our earlier model assumed that the frequency of the key trances at night or in the cold, by adjusting the height or shape resource in the environment depends solely on niche construc- of their mounds to optimize the intake of the sun’s rays, or by tion. This assumption is clearly unrealistic in many cases, carrying their brood around their nest to the place with the because the distributions of ecological resources often depend optimal temperature and humidity for the brood’s develop- on processes that are independent of the population (6, 23). Here we present findings of an analysis with a more complex The publication costs of this article were defrayed in part by page charge treatment of the frequency of the resource in which it is payment. This article must therefore be hereby marked ‘‘advertisement’’ in accordance with 18 U.S.C. §1734 solely to indicate this fact. ‡To whom reprint requests should be addressed. E-mail: PNAS is available online at www.pnas.org. [email protected]. 10242 Downloaded by guest on September 26, 2021 Evolution: Laland et al. Proc. Natl. Acad. Sci. USA 96 (1999) 10243 influenced by varying mixes of a population’s niche- two-locus multiplicative viability model. The frequency- construction and other independent environmental processes dependent components of the contribution to fitness of geno- of renewal or depletion. types AA, Aa, and aa are functions of R, ͌R(1 Ϫ R) and 1 Ϫ R, respectively, chosen so that allele A will be favored by this THE MODEL component of selection when the resource is common and Consider an isolated population of randomly mating, diploid allele a when it is rare. Thus, the frequency-dependent com- individuals, defined at two diallelic loci, E (with alleles E and ponents are functions of the frequency of the resource, mod- e) and A (with alleles A and a). In generation t, the frequencies ified by niche construction. The coefficient of proportionality Ϫ of the four gametes (EA, Ea, eA, and ea) are given by x1t (␧) determines the strength of the frequency-dependent com- x4t, respectively, so that the frequencies of alleles E and A are ponent of selection relative to the fixed-fitness component ϭ ϩ ϭ ϩ pt x1t x2t, and qt x1t x3t. We assume that the (Ϫ1 Ͻ ␧ Ͻ 1). Positive values of ␧ represent cases where an population’s capacity for niche construction is influenced by increase in the amount of resource results in an increment in the frequency of alleles at the E locus. Genotypes at the A locus the fitness of genotypes containing allele A, whereas negative make contributions to the two-locus fitnesses that are functions values of ␧ represent cases where an increase in R favors a. of the frequency with which a resource (R) is encountered in The genotype fitnesses w in Table 1 give rise to the standard Ͻ Ͻ ij their environment (where 0 R 1). This frequency is a gametic recursions function of the amount of niche construction over n genera- ϭ ͓ ͑ ϩ ϩ ϩ ͔͒ Ϫ tions (that is, the frequencies of allele E) as well as other Wx*1 x1 x1w11 x2w21 x3w12 x4w22 rw22D [2a] independent processes of resource recovery or resource dis- ϭ ͓ ͑ ϩ ϩ ϩ ͔͒ ϩ sipation. We define as positive niche construction phenotypic Wx*2 x2 x1w21 x2w31 x3w22 x4w32 rw22D [2b] activities that increase the fitness of the niche-constructing * ϭ ͓ ͑ ϩ ϩ ϩ ͔͒ ϩ organism, whereas negative niche construction refers to niche- Wx 3 x3 x1w12 x2w22 x3w13 x4w23 rw22D [2c] constructing activities that reduce fitness. In our model, pos- Wx* ϭ ͓x ͑x w ϩ x w ϩ x w ϩ x w ͔͒ Ϫ rw D, [2d] itive and negative niche construction, respectively, refer to 4 4 1 22 2 32 3 23 4 33 22 processes that increase and deplete the frequency of a valuable ϭ Ϫ where r is the recombination rate, D x1x4 x2x3 is the resource. This treatment of the interaction between the pop- linkage disequilibrium between the loci, and W is given by the ulation and the resource is still extremely simplified. A more sum of the right-hand sides of Eqs. 2a–2d. realistic treatment would involve general distributions of the resource, more complex ecological dynamics of resource and RESULTS population, and ecological models that take the density of We consider the effects of niche construction under four niche constructors into account (6, 26, 27).
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