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Species Selection on Variability (Hierarchical Selection Theory/Emergent Characters/Aggregate Characters/Adaptation) ELISABETH A

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Species Selection on Variability (Hierarchical Selection Theory/Emergent Characters/Aggregate Characters/Adaptation) ELISABETH A Proc. Natl. Acad. Sci. USA Vol. 90, pp. 595-599, January 1993 Evolution Species selection on variability (hierarchical selection theory/emergent characters/aggregate characters/adaptation) ELISABETH A. LLOYD* AND STEPHEN JAY GOULDt *Department of Philosophy, University of California, Berkeley, CA 94720; and tMuseum of Comparative Zoology, Harvard University, Cambridge, MA 02138 Contributed by Stephen Jay Gould, October 14, 1992 ABSTRACT Most analyses of species selection require Gould, and others (1-7) in several articles have defended the emergent, as opposed to aggregate, characters at the species idea that selection at a particular level requires characters to level. This "emergent character" approach tends to focus on be heritable and emergent at that level and to interact with the the search for adaptations at the species level. Such an ap- environment to cause sorting. Species-level properties are proach seems to banish the most potent evolutionary property divided into aggregate and emergent characters. Aggregate of populations-variability itself-from arguments about spe- characters are based on the inherent properties of subparts cies selection (for variation is an aggregate character). We and are simple statistics of these properties, while emergent wish, instead, to extend the legitimate domain of species characters arise from the organization among subparts (ref. 4, selection to aggregate characters. This extension of selection p. 146). Possible emergent characters among species include theory to the species level wil concentrate, instead, on the population size, distribution, and composition (4). relation between fitness and the species character, whether According to this argument, which we shall call the "emer- aggregate or emergent. Examination of the role of genetic gent character" approach, one need only show that a trait in variability in the long-term evolution of clades illustrates the question is aggregate, not emergent, in order to demonstrate cogency of broadening the definition of species selection to that species are not functioning as units of selection in a include aggregate characters. We reinterpret, in this light, a particular case (1, 2, 4). classic case presented in support of species selection. As We shall contrast the emergent character approach with an originally presented, the species selection explanation ofvolutid "emergent fitness" or "interactor approach," which empha- neogastropod evolution was vulnerable to a counterinterpre- sizes the nature of fitness values, rather than type of char- tation at the organism level. Once this case is recast within a acter. Under this approach (presented in more detail in definition of species selection that reflects the essential struc- Emergent Fitness or Interactor Approach), the relationship ture and broad applicability of hierarchical selection models, between character and environment becomes the key issue. the organism-level reinterpretation ofvariability loses its force. This relationship is represented in the fitness parameters. We conclude that species selection on variability is a major Selection processes are delineated by distinctive attributes of force of macroevolution. the fitness parameters. Interactors, and hence selection pro- cesses themselves, are individuated by the contributions of their traits to fitness values in evolutionary models; the trait Selection itself can be an emergent group property or a simple sum- mation of organismic properties. This definition of an entity We begin with some basic distinctions. Most important is the undergoing selection is much more inclusive than in the difference between a process and an outcome ofthat process; emergent character approach, since an entity might have in this case, selection is the process, and evolutionary change either aggregate or emergent characters (or both); this dis- is the outcome. The process of selection involves an inter- tinction between emergent and aggregate characters does not action between an entity and its environment or, more usually appear in quantitative models of species selection specifically, between a particular trait of an entity and (e.g., see ref. 8). The emergent fitness approach requires only particular aspects of its environment. Part of the fitness that a trait have a specified relation to fitness in order to calculated for an entity represents the particular value con- support the claim that a selection process is occurring at that ferred by having a specific trait in a specific environment. In level (cf. refs. 7, 9, and 10; see Emergent Fitness orInteractor other words, the component offitness associated with a trait Approach and Appendix). is the representation, in an evolutionary model, of the pro- cess of selection. Adaptations The selection process itself must be contrasted with the result or outcome of that process. Sorting is simply the An important component ofthe emergent character approach differential birth and death of individual entities in a popu- is its focus on adaptations. The existence of an emergent lation, while selection is a potential cause ofthat sorting (ref. character at the species level is taken as equivalent to the 1, p. 217). Sorting at a particular level has a variety of existence of a potential species-level adaptation (ref. 11, p. potential causes; it can arise from selection acting at that level 388; ref. 12, p. 132). or occur as a consequence ofchance or of selection processes The focus on characters rather than fitnesses is related to at either a higher or a lower level. this requirement for adaptations. Emergent characters are always potential adaptations. Not all selection processes Species Selection produce adaptations, however. The key issue, in delineating a selection process, is the relationship between a character A number of attempts have been made to apply the basic and fitness. The emergent character approach is more re- notion of selection to the species level. Vrba, Eldredge, strictive than alternative schemas that delineate selection processes, for only some selection processes at the species The publication costs of this article were defrayed in part by page charge level (perhaps very few) result in the evolution of emergent payment. This article must therefore be hereby marked "advertisement" characters or adaptations. The emergent character approach in accordance with 18 U.S.C. §1734 solely to indicate this fact. picks out a subset of cases given by the interactor approach; 595 Downloaded by guest on September 30, 2021 596 Evolution: Lloyd and Gould Proc. Natl. Acad. Sci. USA 90 (1993) it is, to be sure, an especially interesting subset-namely, this case. This is done by describing interactors at the lower species-level adaptations. Nevertheless, if one is interested level first. If a higher-level interactor exists, the higher-level in discussing evolution by species-level selection processes correlation offitness and trait will appear as a residual fitness per se, then this approach is too restrictive.t Let us return to contribution at the lower level; we must then go to the higher the emergent fitness approach to see how aggregate traits, level in order to represent the correlation between higher- which are not adaptations, could function in a species selec- level trait and higher-level fitness. Hence, species-level fit- tion process. ness is not defined as an average or sum of the organismic fitnesses within a species (see refs. 7, 10, and 19). Emergent Fitness or Interactor Approach More simply put-the operative notion in all examples of higher-level selection is some sort of interaction effect or As the guiding idea behind our hierarchical view of selection context dependence (e.g., ref. 20; see ref. 21, chapt. 7; here, models, we hold that selection processes are best described "context" refers to the other entities in the same population in terms of interactors (see refs. 15-17). An interactor is an and not to the environment). Intuitively, the properties ofthe entity that has a trait; the interactor must interact with its other members of your group must make a difference, and environment through the trait, and the interactor's expected there must be a correlation between group type and fitness. survival and reproductive success are determined, at least One might object that the above approach to delineating partly, by this interaction. In other words, the interactor's interactors is overly reductionist. After all, it seems that this fitness covaries with the trait in question. view simply embodies G. C. Williams's famous and mislead- If we have an interactor, we should expect to find a ing maxim: don't even consider any higher level of selection correlation between the interactor's trait and the interactor's unless the lower-level model proves empirically inadequate fitness.§ For evolution by selection to occur, both the trait (ref. 22, p. 55). The problem with Williams's maxim is that and the correlation between trait and fitness must be at least different selection processes may sometimes yield identical partly heritable (in the sense of narrow heritability). Herita- gene frequency predictions. In these cases, additional infor- bility depends, in turn, on the additive genetic variance ofthe mation about population structure, group membership, and trait by definition. It should be recalled that fitness itself can group-level fitnesses is needed in order to tell which model be analyzed into components, each correlated with a trait that best fits the system at hand (see ref. 19, pp.
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