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Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):11904-9.

Individuality and adaptation across levels of selection: how shall we name and generalize the unit of Darwinism?

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Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA.


Two major clarifications have greatly abetted the understanding and fruitful expansion of the theory of natural selection in recent years: the acknowledgment that interactors, not replicators, constitute the causal unit of selection; and the recognition that interactors are Darwinian individuals, and that such individuals exist with potency at several levels of organization (genes, organisms, demes, and species in particular), thus engendering a rich hierarchical theory of selection in contrast with Darwin's own emphasis on the organismic level. But a piece of the argument has been missing, and individuals at levels distinct from organisms have been denied potency (although granted existence within the undeniable logic of the theory), because they do not achieve individuality with the same devices used by organisms and therefore seem weak by comparison. We show here that different features define Darwinian individuality across scales of size and time. In particular, species-individuals may develop few emergent features as direct adaptations. The interactor approach works with emergent fitnesses, not with emergent features; and species, as a consequence of their different mechanism for achieving individuality (reproductive exclusivity among subparts, that is, among organisms), express many effects from other levels. Organisms, by contrast, suppress upwardly cascading effects, because the organismic style of individuality (by functional integration of subparts) does not permit much competition or differential reproduction of parts from within. Species do not suppress the operation of lower levels; such effects therefore become available as exaptations conferring emergent fitness-a primary source of the different strength that species achieve as effective Darwinian individuals in evolution.

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