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The Neutral Theory of Biodiversity and Biogeography and Stephen Jay Gould Author(S): Stephen P The neutral theory of biodiversity and biogeography and Stephen Jay Gould Author(s): Stephen P. Hubbell Source: Paleobiology, 31(sp5):122-132. 2005. Published By: The Paleontological Society DOI: 10.1666/0094-8373(2005)031[0122:TNTOBA]2.0.CO;2 URL: http://www.bioone.org/doi/full/10.1666/0094- 8373%282005%29031%5B0122%3ATNTOBA%5D2.0.CO%3B2 BioOne (www.bioone.org) is an electronic aggregator of bioscience research content, and the online home to over 160 journals and books published by not-for-profit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Paleobiology,31(2, Supplement),2005,pp.122±132 The neutral theory of biodiversity and biogeography and Stephen Jay Gould Stephen P. Hubbell Abstract.ÐNeutral theory in ecology is based on the symmetry assumption that ecologically similar species in a community can be treated as demographically equivalent on a per capita basisÐequiv- alent in birth and death rates, in rates of dispersal, and even in the probability of speciating. Al- though only a ®rst approximation, the symmetry assumption allows the development of a quan- titative neutral theory of relative species abundance and dynamic null hypotheses for the assembly of communities in ecological time and for phylogeny and phylogeography in evolutionary time. Although Steve Gould was not a neutralist, he made use of ideas of symmetry and of null models in his science, both of which are fundamental to neutral theory in ecology. Here I give a brief over- view of the current status of neural theory in ecology and phylogeny and, where relevant, connect these newer ideas to Gould's work. In particular, I focus on modes of speciation under neutrality, particularly peripheral isolate speciation, and their implications for relative species abundance and species life spans. Gould was one of the pioneers in the study of neutral models of phylogeny, but the modern theory suggests that at least some of the conclusions from these early neutral models were premature. Modern neutral theory is a remarkably rich source of new ideas to test in ecology and paleobiology, the potential of which has only begun to be realized. Stephen P. Hubbell. Department of Plant Biology, University of Georgia, Athens, Georgia 30602, and Smithsonian Tropical Research Institute, Unit 0948, APO AA 34002-0948. E-mail: [email protected] Accepted: 12 September 2004 Introduction generates a set of formal null hypotheses for the origin, maintenance, and loss of species in Many of Gould's ideas generated controver- ecological communities or in phylogenies sy, but one for which he was never criticized (Hubbell 2001a). Gould understood the criti- was being a neutralist, which he most de®- cal importance of null models in his own sci- nitely was not. On the contrary, Gould argued ence (Gould et al. 1977), and in science in gen- that patterns of punctuated equilibria in phy- eral. He also understood their importance as logeny can be explained only if natural selec- a control on one's own preconceptions and bi- tion operates not just among individuals with- ases, and what can happen when such con- in populations, but also among species and trols are absent or abused, as in the racist the- higher taxon levels (Gould 2002). Selection op- ories of human evolution, which Gould vig- erating at levels above the individual would of orously refuted (Gould 1981). In the 1970s, course imply that species and higher taxa dif- Gould and his collaborators used null models fer in fundamental ways that affect their rel- of phylogeny as a means to evaluate whether ative ®tnesses on geological timescales, which the patterns generated solely by random birth- in turn affect their relative life spans in the fos- death processes were consistent with the sil record. punctuated equilibrium hypothesis of evolu- Although Gould was not a neutralist, there tion, with busts of speciation interspersed are at least two deep philosophical connec- with long periods of relative quietude (Raup tions between Gould and current neutral the- et al. 1973; Gould et al. 1977). They found that ory. The ®rst is his recognition of the impor- randomly generated patterns were not consis- tance of null models in science, and more spe- tent with observed patterns, and so Gould and ci®cally Gould's pioneering work using neu- company concluded that non-neutral selection tral models to study phylogeny. The uni®ed processes must be at work in the phylogenies neutral theory of biodiversity and biogeogra- he studied. As it turns out, however, these phy is a recent example of such models, and it conclusions were somewhat premature, be- q 2005 The Paleontological Society. All rights reserved. 0094-8373/05/3102-0009/$1.00 GOULD AND NEUTRAL THEORY 123 cause there were several problems with the The Neural Theory and Relative formulations of the models that were not im- Species Abundance mediately apparent at the time. The origins of modern neutral theory in The other philosophical connection of neu- ecology can be traced back to the theory of is- tral theory to Gould is through the concept of land biogeography (MacArthur and Wilson symmetry and symmetry breaking. In the 1963, 1967). The theory of island biogeogra- neutral theory of biodiversity, all species are phy hypothesizes that ecological communities treated as symmetric, which means that, to a are assembled purely by dispersal. This and ®rst approximation, all species are assumed to other dispersal assembly theories assert that be demographically identical on a per capita the species richness on islands or in local com- basis. The principal use of the neutral theory munities represents a dynamic equilibrium is to evaluate when, and to what degree, asym- between the rates of immigration of species metries among species are required to explain into the community and the rate of their sub- the assembly of observed ecological commu- nities. Although Gould did not use this ter- sequent local extinction. Thus, such theories minology, nevertheless the concepts he wrote assert that communities are in taxonomic non- about were the same. Paleontology could be equilibrium with continual species turnover. described as the study of how morphological The theory of island biogeography is neutral symmetries are transmitted, broken, and re- because it assumes that species are identical established over evolutionary time. In phylog- (symmetric) in their probabilities of arrival enies, more closely related species are more and survival. This theory was, and remains, a similar (symmetric) than less related species radical departure from most contemporary (Harvey and Pagel 1991). At least for the living theory in ecology, which says that ecological species, the new tools of genomics and evo- nature is fundamentally asymmetric, that lutionary developmental biology promise to communities are equilibrium or near-equilib- answer many if not all of the recalcitrant clas- rium assemblages of niche-differentiated spe- sic questions in ontogeny and phylogeny cies, each of which is the best competitor in its (Gould 1977). These tools are revealing that own ecological niche (Chase and Leibold the symmetries of life run far deeper than any- 2003). There has been a persistent theoretical one ever supposed, as illustrated, for example, tension in ecology between these two con¯ict- by the discovery of ancient and phylogeneti- ing worldviews. Both perspectives have cally pervasive homeobox master regulatory strong elements of truth, although typically on genes (Carroll et al. 2001; Davidson 2001). very different spatial and temporal scales In this paper, I ®rst present a brief synopsis (Hubbell 2001a). The theoretical quest has of the neutral theory (Hubbell 2001a; Volkov been the search for ways to reconcile and com- et al. 2003). The current theory is best devel- bine these divergent perspectives into a single oped for ecological scales of time and space. seamless theory for ecology. However, the uni®ed neutral theory embodies The uni®ed neutral theory of biodiversity more of a macroecological and deep-time per- begins to build a theoretical bridge between spective than do most contemporary theories these two perspectives by incorporating a dy- in ecology. This is because it is one of very few namic theory of relative species abundance theories in ecology to incorporate a process of into the theory of island biogeography (Hub- speciation explicitly. Here I focus mainly on bell 2001a; Bell 2000, 2001). As in the original the results for speciation, particularly periph- theory, the uni®ed neutral theory treats spe- eral isolate speciation, and its implications for cies as identical (symmetric) in their per capita biodiversity, speciation rates, and species life vital rates of birth, death, and migration. Un- spans. I conclude with a brief prospect for the like the theory of island biogeography, how- future of symmetric neutral theory in ecology ever, the uni®ed neutral theory makes the and paleobiology, and how new models with neutrality assumption at the individual level, symmetry broken in various ways promise to not the species level, a change that allows spe- move us forward. cies to differentiate in relative abundance 124 STEPHEN P. HUBBELL through ecological drift (demographic sto- chasticity). The persistence times of species under drift are then dictated by their abun- dances, so that the extinction rate is a genuine prediction of the theory, not a free parameter as it was in the original theory of island bio- geography.
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