Multilocus genetic structure of ancestral Spanish and colonial Californian populations of Avena barbata

We have applied a multivariate log-inear technique to the analysis ofinterlocus allelic associations among 14 allozyme loci in a sample of 4011 plants from 42 Spanish populations of Avena barbata. The loci fell into three natural groups of five, five, and four loci. The five loci of the first group are invariant, or nearly so, throughout the range ofthe species. The genetic organization of the loci of this set is defined by a single five-locus genotype; each allele of this predominant genotype is a "wild-type" allele that contributes favorably to adaptedness in all single-locus and multilocus configurations regardless of environment. Although allelic diversity is high in Spain for the nine loci of the second and third sets, log-linear analyses showed that these loci are tied together in Spanish populations through complex networks of overlapping lowerorder interlocus interactions. The ancestral Spanish and colonial Californian gene pools are closely similar in allelic composition on a locus-by-locus basis; however, Spanish allelic configurations at two-locus and higher-order levels are usually different from and much less tightly organized than in Californian populations. We conclude that the major force involved in the evolution of the colonial populations was selection that led to reorganization, at the interlocus level, of the ancestral Spanish alelic ingredients into different multilocus genotypes adapted to Californian habitats. The Slender Wild Oat, Avena barbata Pott ex Link. , is a diploidized tetraploid grass that is distributed over a vast area from the Western Mediterranean Basin across the Middle East to Nepal (1). Historical records indicate that A. barbata was introduced to California from Spain in the period of exploration and colonization and that the species soon became a major component of a number of distinct habitats in California (2). Detailed studies of the ecogenetics of A. barbata in California (3) have established that the species is now differentiated into several ecotypes marked by specific multilocus combinations of alleles of discretely identifiable morphological, allozyme, and restriction-fragment variants and that these ecotypes are distributed in patterns that precisely overlay environmental heterogeneity, especially heterogeneity for available moisture and for temperature. A. barbata occurs in two major climatic zones in California (4), the Mediterranean hot summer zone, which includes the extensive semiarid grasslands and oak savannah of the foothills bordering the Central Valley, and the Mediterranean cool summer zone, which includes the intermontane regions of the Pacific coastal strip and the higher foothills of the Sierra Nevada mountains; the Mediterranean cool summer zone is characterized by mild wet winters and a diversity of habitats varying from mesic to semiarid. The great majority of populations in the hot summer zone are nearly monomorphic for a specific combination of alleles designated xeric, The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact. whereas most populations in the cool summer zone are nearly monomorphic for a constellation of alleles designated mesic. In areas of interface between semiarid and mesic habitats, zones of polymorphism for xeric and mesic gametic types occur on a microgeographical scale, in which frequencies of the two gametic types are correlated with available moisture and temperature. Gametic types featuring mixtures of xeric and mesic alleles are rare (3). Also the size of xeric and mesic zones expands and contracts, and the frequencies of xenc and mesic gametic types shift rapidly in polymorphic zones in dry and wet years. A dozen or so additional ecotypes, each marked by a specific set of multilocus allelic complexes, have been identified in California; these ecotypes generally occupy small patches featuring unusual edaphic conditions. It is apparent from a recent detailed study (5) of42 Spanish populations of A. barbata that present-day Spanish and Californian populations are closely similar in allelic composition and allelic frequencies but that the arrays of multilocus genotypes found in the colonial gene pool are different from those of the ancestral Spanish gene pool. Main objectives of the present study were to determine whether ecotypes parallel to those marked by multilocus complexes of alleles in California also occur in Spain and whether rainfall and temperature are major environmental factors in Spain as in California. Genetic structure among loci has conventionally been assessed in terms of pairs of loci; however, two-locus measures are inadequate for analysis of multilocus structure, and we have consequently used a discrete multivariate loglinear technique (6), as adapted for study of associations among several loci with each other and with environmental factors (7), in our analyses of the Spanish multilocus A. barbata data. We conclude from our analyses that the present-day Spanish and Californian gene pools are differently structured on a multilocus basis and that the main force responsible for evolutionary change in the colonial populations was selection for particular combinations of alleles at many different loci that allowed the colonial populations to meet the different environmental challenges encountered in California. MATERIALS AND METHODS The materials of this study were the same 4011 plants collected from 42 Spanish populations located at sites illustrated in figure 1 of ref. 5. Each site was sampled by collecting a single panicle from -100 randomly chosen individuals. A single seed was sown from each panicle, and crude extracts from seedlings were assayed electrophoretically and scored for 14 allozyme loci; the 51 allozyme alleles and 80 homozygous single-locus allozyme genotypes observed in the 4011 individuals scored are described in ref. 5. The number of possible 14-locus genotypes is several orders of magnitude tPresent address: Department of Agronomy and Range Science, University of California, Davis, CA 95616.