The California population of Agaricus bisporus comprises at least two ancestral elements

Genotypes of a sample of field-collected heterokaryon isolates of Agaricus bisporus from California were compared with those of a comprehensive sample of cultivar isolates that are likely to be of European ancestry. Isolate genotypes were determined for 14 nuclear DNA restriction fragment length polymorphism markers and seven allozyme markers, and were compared in a pairwise fashion to produce a matrix of genotypic dissimilarities between all isolates. This matrix was evaluated with regard to the affinities of individual California isolates, both among themselves and with a reconstructed population ancestral to the cultivars. Most isolates from California fell into one of two apparent groups; these either: 1) had high affinity with the cultivars or 2) differed substantially from the cultivars and aggregated in a distinct, cypress-associated "Californian" group. A few isolates had an intermediate character. This result, supported by habitat correlations and the distribution of characteristic mitochondrial DNA types, indicates that the California population presently comprises introduced cultivars, indigenous cypress-associated strains, and a less distinct group that could include spontaneous hybrids between these two ancestral elements, or strains with other affinities. If hybridization is indeed occurring, the two major ancestral elements have introgressed only slightly. Agaricus bisporus (Lange) Imbach, the familiar "Button Mushroom" of commerce (for nomenclatural debate see Kerrigan 1987; Malloch et al. 1987), is now cultivated on six continents. Little is known, however, about natural populations of this species. Historical evidence strongly indicates that most or all cultivar lines were selected, over the last three centuries, from wild mushrooms collected in Europe, often found in association with accumulations of horse manure or other agricultural wastes (Falconer 1891; Robinson 1870). Genetically, cultivar isolates form a relatively homogeneous group, which also suggests that they were originally drawn from a single population or gene pool (Kerrigan 1990; May and Royse 1982; Royse and May 1982a). Cultivars are known to have become naturalized in North America, based on analysis of genetic markers in field-collected isolates (Kerrigan and Ross 1989, and below). Dispersal of germ plasm has apparently been exclusively unidirectional, from Europe; to our knowledge no foreign germ plasm had been sent to Europe prior to our distribution of research cultures beginning in 1989. As a result of this asymmetry, a sample of the (European) A. bisporus population from which the cultivar stocks were drawn can plausibly be reconstructed from extant cultivars. In contrast, field samples from almost any other region could include elements having either cultivar, indigenous, or hybrid ancestry. The possible existence of indigenous, non-European populations of A. bisporus, and even the status of the organism as a "natural species", have been called into question (May and Royse, 1982; Raper et al. 1972). Morphologically, the species concept is well delimited, as this is the only known species of Agaricus with predominately bisporic basidia. The possibilities of multiple independent origins of this trait, or of divergence into reproductively isolated biological species, have not previously been addressed. Evidence from six allozyme loci for the existence in California of an indigenous, non-cultivar population of A. bisporus was presented by Kerrigan and Ross (1989). Studies of A. bisporus populations are complicated by the unpredictability of the occurrence of the ephemeral sporocarps, by which individual mycelia are located, and by the fact that over the great majority of its range, the species is only very occasionally encountered. This suggests that population densities may typically be low, relative to many