SPECIAL FEATURE Community Genetics: New Insights into Community Ecology by Integrating Population Genetics1 Community genetics is the study of the interaction between genes within a species and pop- ulations of other species in a community. This area of research was ®rst introduced by Janis Antonovics (1992 [Toward community genetics. Pages 426±429 in R. S. Fritz and E. L. Simms, editors. Plant resistance to herbivores and pathogens: ecology, evolution and genetics. University of Chicago Press, Chicago, Illinois, USA]) as a modern attempt to integrate community ecology and evolution. Research programs in community genetics span from understanding the mechanistic bases of the evolution of organisms in a community context to identifying the role of genetic variation in generating community patterns. Is community genetics an emerging subdiscipline that ®nally unites multispecies ecology with the genetics of evolutionary change? It is argued that a mature understanding of either ecological communities or the evolution of species will require community genetics. Others cry that this label is nothing more than funding-agency-style renaming of perfectly good, classic questions in evolutionary ecology. I have asked two of the leading groups in community genetics to lay down the de®nitions and set the agenda for future work: Neuhauser et al., who established a Center for Community Genetics at the University of Minnesota; and Whitham et al., who have been studying the consequences of genetic variation for diverse communities and community processes. The result is two fresh and controversial lead papers. Following these papers are commentaries from eight respondents. Some of these authors were pioneers in bridging the ®elds of community ecology and evolution; others are newcomers seeking to infuse ecology with novelty. The result is a mix of arguments that illustrate the vigorous debate within modern community ecology. The feature starts and ends with perspectives articulated by Janis Antonovics. Neuhauser et al. and Whitham et al. loosely follow Antonovics's (1992) reductionist and holist perspectives, respectively. The hallmark of the reductionist approach (Neuhauser et al.) is to document rapid evolutionary change. As nonequilibrial communities are affected by anthropogenic or other in- ¯uences, strong interactions catalyze ¯ux in abundances of individuals in multispecies commu- nities, and these changes can rapidly alter the genetics of community members. It is argued that incorporation of spatial dynamics and population biology in interacting species is necessary to predict the eventual ecological and evolutionary outcome of perturbation. On the holistic side (Whitham et al.), the goal is to understand the consequences of particular genes (or gene com- binations) in a community on higher levels of biological organization. Here, the in¯uence of particular genetic variants on communities and ecosystem properties is examined in more or less equilibrial communities. Variation generated by hybridization between species has been the pri- mary tool used to study the role of particular genes on communities; little is currently known about the role of variation within a single species. In addition, the role of genetic variance or diversity in a population in generating higher-level community properties such as productivity and species diversity is a central goal of the holistic approach to community genetics. Perhaps nobody could cogently argue that ecology and evolution can be disciplines without each other. Yet the respondents disagree in terms of the projected role for community genetics in ecology. Tension persists over the possibility of natural selection acting on levels higher than the individual. There is a persuasive call for examining and accounting for the in¯uence of interspeci®c (phylogenetic) relatedness within community studies. Add all this to the nagging age-old questions of how to de®ne a community, who the important dominant or keystone members are, and how to assess the relative importance of various factors in¯uencing community structure. 1 Reprints of this 59 page Special Feature are available for $9.75 each, either as pdf ®les or as hard copy. Prepayment is required. Order reprints from the Ecological Society of America, Attention: Reprint Department, 1707 H Street, N.W., Suite 400, Washington D.C. 20006 (e-mail: [email protected]). 543 Although we may be able to agree that it is a worthy goal to integrate more than one or two species into the study of population genetic change and to integrate genetics into the study of community patterns, will the reductionist and holistic approaches ever meet? Perhaps the study of coevolution in real communities (diffuse coevolution) will be the ®rst benefactor of the com- bined reductionist and holistic approaches to community genetics. Others will soon follow. Ul- timately, the goal is to develop an increasing ability to describe and predict patterns in nature. ÐANURAG A. AGRAWAL, Special Features Editor Key words: coevolution; diversity; group selection; intraspeci®c variation; multilevel selection; phy- logenetics of communities; population genetics; species richness. q 2003 by the Ecological Society of America Special Feature Ecology, 84(3), 2003, pp. 545±558 q 2003 by the Ecological Society of America COMMUNITY GENETICS: EXPANDING THE SYNTHESIS OF ECOLOGY AND GENETICS CLAUDIA NEUHAUSER,1,4,5 D. A. ANDOW,2,4 GEORGE E. HEIMPEL,2,4 GEORGIANA MAY,1,4 RUTH G. SHAW,1,4 AND STUART WAGENIUS3,4 1Department of Ecology, Evolution and Behavior, University of Minnesota, 100 Ecology Building, 1987 Upper Buford Circle, St. Paul, Minnesota 55108 USA 2Department of Entomology, University of Minnesota, 1980 Folwell Ave, St. Paul, Minnesota 55108 USA 3Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, Illinois 60022 USA 4The Minnesota Center for Community Genetics, University of Minnesota, St. Paul, Minnesota 55108 USA Abstract. Community genetics synthesizes community ecology and population genetics and yields fresh insights into the interplay between evolutionary and ecological processes. A community genetics framework proves especially valuable when strong selection on traits results from or impinges on interspeci®c interactions, an increasingly common phenomenon as more communities are subject to direct management or anthropogenic disturbances. We draw illustrations of this perspective from our ongoing studies of three representative communities, two managed and one natural, that have recently undergone large perturba- tions. The studied communities are: (1) insect pests of crop plants genetically engineered to produce insecticidal toxins; (2) insect-pollinated plants in habitats severely fragmented by agriculture and urbanization; and (3) a pathogen and its crop host now grown extensively outside their native ranges. We demonstrate the value of integrating genetic and ecological processes to gain a full understanding of community dynamics, particularly in nonequilib- rium systems that are subject to strong selection. Special Feature Key words: anthropogenic disturbance; Bt maize; community genetics; Echinacea angustifolia; evolution of resistance; genetic engineering; habitat fragmentation; nonequilibrium dynamics; plant± insect interactions; plant±pathogen interactions; Ustilago maydis. INTRODUCTION a given place. The strength of interaction between members of a community varies. Strong interactions Janis Antonovics (1992) articulated a vision for a can arise even for species that have associated only new ®eld of inquiry, ``community genetics'' (a term recently. For example, in the case of species invasions, suggested by Dr. J. P. Collins, Arizona State Univer- strong interactions may be apparent from the time that sity), to investigate the ``role of genetic variation in a species arrives at a given location (Pritchard and in¯uencing species interactions and determining com- Schluter 2001). Assembly of novel communities may munity structure.'' Community genetics is a synthesis have evolutionary, as well as ecological, consequences of community ecology and evolutionary genetics; it within few generations (Reznick et al. 1997, 2001, Da- directly assesses the interplay between genetic varia- vis and Shaw 2001). When, in addition, ecological in- tion and community dynamics to develop a mechanistic teractions strongly in¯uence the genetic composition understanding of the evolution of organisms in the con- of populations, the conceptual framework of commu- text of the communities that they occupy. nity genetics becomes valuable. Our community concept is that developed by Glea- Community genetics addresses questions about the son (1917, 1926, 1927), demonstrated by Whittaker evolution of interactions among organisms in a broader (1956), and supported by the work of Davis (1981) on context than that of the more stringent framework of community assembly. In this concept, species assemble coevolution where ``an evolutionary change in a trait in communities according to their individualistic attri- . in one population in response to . a second butes. We superimpose on this concept a contemporary population, [is] followed by an evolutionary response understanding of the ubiquity of genetic variation. by the second population to the change in the ®rst'' Thus, a community is the multispecies assemblage of (Janzen 1980). A situation in which the ecological suc- genetically variable populations that together occupy cess of one species depends on the genotypes of a sec- ond species would not necessarily