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Neutral Theory in Macroecology and Population Genetics

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Neutral Theory in Macroecology and Population Genetics FORUM is intended for new ideas or new ways of interpreting existing information. It FORUM provides a chance for suggesting hypotheses and for challenging current thinking on FORUM ecological issues. A lighter prose, designed to attract readers, will be permitted. Formal research reports, albeit short, will not be accepted, and all contributions should be concise FORUM with a relatively short list of references. A summary is not required. OIKOS 00: 00Á/00, 2006 DOI: 10.1111/j.2006.0030-1299.14837.x Neutral theory in macroecology and population genetics Xin-Sheng Hu and Fangliang He, Dept of Renewable Resources, 751 General Service Building, Univ. of Alberta, Edmonton, Alberta, Canada, T6G 2H1 ([email protected]). / Stephen P. Hubbell, Dept of Plant Biology, Univ. of Georgia, Athens, GA 30602, USA, and also: Smithsonian TropicalÁ Research Institute, Unit 0948, APO AA 34002-0948. Current neutral theory in macroecology has many parallels with tive, testable null hypotheses in community ecology, neutral theory in population genetics, but it also has many distinct biogeography and conservation biology, particularly in features that arise because it focuses mainly on questions at the community level rather than at the population level. Here we communities whose explicit spatial characteristics or highlight the similarities and differences between these two bodies physical barriers play a role. The neutral theory is a of theories from the aspects of the operational units, definitions of null hypothesis because it assumes there are no neutrality, basic parameters, driving forces, spatial structure and differences among individuals in terms of per capita community assembly rules. Compared with neutral theory in population genetics, whose development spans more than 40 years, vital rates or in their responses to the basic forces neutral theory in ecology, which is only a few years old, is still acting on a community. Neutral macroecology provides immature and under-developed. There are many opportunities for insights into the ecological and evolutionary processes major theoretical contributions, some of which can be adopted directly from population genetics, while others will require new that control the assembly and dynamics of the meta- theoretical work. We critically discuss these opportunities and community and of local communities, including the theoretical challenges in neutral macroecology, particularly in roles of dispersal, ecological drift, and speciation. The regard to effective community size, ecological drift, community differentiation and ecological dominance. metacommunity is the evolutionary biogeographic unit in which member species originate, live and eventually go extinct. The metacommunity can be subdivided into The recent development of neutral theory in macro- ‘‘a set of local communities that are linked by dispersal ecology provides a tractable null hypothesis for testing of multiple potentially interacting species.’’ (Leibold et community assembly rules (Caswell 1976, Bell 2001, al. 2004) or a network of communities linked by the Hubbell 2001). As happened early on to neutral theory exchange of migrants (Mouquet and Loreau 2002). in population genetics (Ohta and Gillespie 1996), Like the dynamics of a subpopulation in metapopula- neutral macroecology has also had its critics (Zhang tion (Hanski 1998), a local community in metacommu- and Lin 1997, Yu et al. 1998, Clark and McLachlan nity has a probability of extinction and can be re- 2003, McGill 2003, Ricklefs 2003, Chase 2005, Nee colonized by the dispersing individuals from neighbour 2005). However, neutral theory in macroecology is still communities. Member species in a community are very much a work in progress and advances in the sympatric and trophically similar and they actually or theory are just starting to appear (Chave and Leigh potentially compete for the same or similar resources 2002, Condit et al. 2002, Vallade and Houchmandza- (Hubbell 2001). deh 2003, Volkov et al. 2003, 2005, Alonso and The basic assumption of neutral theory in macroecol- McKane 2004, Etienne and Olff 2004, Etienne 2005, ogy is that all individuals in the community have He 2005, He and Hu 2005, Nee 2005). The neutral equal vital rates of death, birth, immigration, emigra- theory should facilitate the development of quantita- tion, and even an equal probability of becoming a new Accepted 9 January 2006 Subject Editor: Esa Ranta Copyright # OIKOS 2006 ISSN 0030-1299 OIKOS 00:0 (2006) Online Early (OE): OE-1 species (Hubbell 2001). By making the neutrality both ecologists and population geneticists. These con- assumption at the individual level rather than at the nections lead to an appreciation of how current neutral species level, a neutral theory of relative species abun- macroecology can gain from insights derived from the dance becomes possible within the context of the theory classical neutral theory in population genetics. Neutral of island biogeography, which originally defined neu- theory in macro-ecology has already generated a rich trality at the species level (MacArthur and Wilson 1967, array of null hypotheses, but the unexplored connections Hubbell 2001). The central themes of community to theory in population genetics promise to generate ecology could then be reinterpreted, resulting in new even more, and stimulate discussion on new theoretical explanations for the origin of a variety of macroecolo- directions in macroecology. gical patterns, including species richness, relative Compared with the development of neutral theory in species abundance, species-area relationships, b-diversity population genetics, which has a 40-year history, and phylogeny (Caswell 1976, Bell 2001, Hubbell 2001, the application of the much younger neutral theory in Chave and Leigh 2002, Condit et al. 2002, Zillio ecology has only just begun and some areas remain et al. 2005). largely or wholly undeveloped. While the linkage be- Population genetics and macroecology share a com- tween these two bodies of theories has been recognized mon goal to understand how the spatial and temporal (Caswell 1976, Bell 2001, Hubbell 2001, Chave 2004, patterns of diversity (alleles and species) are formed and Etienne and Alonso 2005, Vellend and Geber 2005) maintained. The development of neutral macroecology and some aspects of differences are also discussed is inspired by population genetics; Hubbell (2001) (Nee 2005), a more detailed comparison has not yet explicitly adopted the analytical strategy used by Ewens been made. Here we summarize the similarities and (1972), i.e. the ‘‘infinite allele model’’, to derive the differences between these two neutral theories, as relative species abundance and speciesÁ/area relation- shown in Table 1. Since most of the items in Table 1 ships at the speciation (mutation)Á/extinction equili- are self-explanatory, here we focus on comparing two brium. However, with the exception of this theoretical critical items relevant to driving forces and spatial link, the broader theoretical connection of neutral structure that have not been much discussed so far macroecology to existing neutral theory in population but are important to understanding community assem- genetics remains largely unexplored. Several major blage. We then highlight some fundamental challenges conceptual connections between these two bodies of and new directions in applying the neutral theory to theory can be made that are of central importance to macroecology. Table 1. A comparison between population genetics and neutral macroecology. Items Population genetics Macroecology Operational units Population Metacommunity subdivision Subpopulations Local communities focal unit Gene Species observed data Allele frequency Species abundance Neutral definition Alleles are selectively neutral, selection Individuals have equal vital rates coefficient:/0, orB/1/2Ne Driving forces Genetic drift (1/2Ne) Ecological drift (1/JM or 1/JL) Mutation Speciation Gene flow among subpopulations Dispersal among local communities Spatial structure Population genetic structure Species distribution and abundance variation among local communities model Island model Island biogeography Stepping stone model Isolation by distance Dispersal limitation Mainland -island Metacommunity-local community Cline pattern (speciation phases) measurement 1/Fis a-diversity Fst b-diversity Spatial autocorrelation Species-area power law Parameters u/4Nev u/2JMvor2JLv Average number of migrants (Nem) Average number of migrants (JLm) Effective population size (Ne) Effective community size (JM or JL) Distribution of allele frequency Distribution of species abundance Fixed (extinct) probability of an allele Fixed (extinct) probability of a species Times to equilibrium or extinction Times to equilibrium or extinction for a mutant of a species Assembly rules Genetic drift/mutation Ecological drift/speciation Genetic drift/migration Ecological drift/dispersal Genetic drift/migration/mutation Ecological drift/dispersal/speciation 2-OE OIKOS 00:0 (2006) Similarities and differences assumption or a mathematical condition for a stable distribution of species abundance (Hubbell 2001). Note Driving forces that the sampling process is assumed to be based on the The dynamics of a neutral allele in a population without total number of individuals, not on the number of species, subdivision is governed by mutation and genetic drift. In in communities. Hence species having low abundances are more likely to go extinct. the infinite allele model, old alleles
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