Geographically structured host specificity is caused by the range expansions and host shifts of a symbiotic fungus

Abstract

The inability to associate with local species may constrain the spread of mutualists arriving to new habitats, but the fates of introduced, microbial mutualists are largely unknown. The deadly poisonous ectomycorrhizal fungus Amanita phalloides (the death cap) is native to Europe and introduced to the East and West Coasts of North America. By cataloging host associations across the two continents, we record dramatic changes in specificity among the three ranges. On the East Coast, where the fungus is restricted in its distribution, it associates almost exclusively with pines, which are rarely hosts of A. phalloides in its native range. In California, where the fungus is widespread and locally abundant, it associates almost exclusively with oaks, mirroring the host associations observed in Europe. The most common host of the death cap in California is the endemic coast live oak (Quercus agrifolia), and the current distribution of A. phalloides appears constrained within the distribution of Q. agrifolia. In California, host shifts to native plants are also associated with a near doubling in the resources allocated to sexual reproduction and a prolonged fruiting period; mushrooms are twice as large as they are elsewhere and mushrooms are found throughout the year. Host and niche shifts are likely to shape the continuing range expansion of A. phalloides and other ectomycorrhizal fungi introduced across the world.

Figure 1

(a) Frequency of host associations across the native (European) and introduced (North American) ranges of A. phalloides. (b) West Coast data are divided into California and the Pacific Northwest to show that in California the dominant hosts are Quercus spp., whereas in the Pacific Northwest dominant hosts are from a mix of introduced angiosperm genera (see text for details). n=number of populations from each region.

Figure 2

δ¹³C ‰ and δ¹⁵N ‰ of mushrooms collected in Europe, the East Coast of North America and California. Each data point represents a single mushroom. Values with standard error bars represent mean values for all mushrooms from each region (±1 s.e.).

Figure 3

(a) Mean mushroom biomass and (b) timing of reproduction of A. phalloides across four biogeographic regions; n=number of populations from each region. Error bars represent ±1 s.d. from the mean. In b, individual gray circles represent the mean value. Sampling intensity varies across different regions, but is proportional to the number of known populations in each region (Wolfe et al., 2010). PNW, Pacific Northwest region of North America. Fruiting date indicates the day of the year (1 to 365).

Figure 4

Host selectivity of A. phalloides at three sites on the Point Reyes Peninsula in Marin County, California, USA. Map shows peninsula shaded with distributions of the dominant EM host species (Q. agrifolia, P. muricata and Pseudotsuga menziesii). Graphs show the available root community and the percent of the total number of A. phalloides root tips where each species was detected as a host.

Figure 5

Distribution of A. phalloides throughout California and the geographic ranges of associated host plants. A significant association between the distribution of A. phalloides and a host range is marked by the thicker borders around Q. agrifolia, C. cornuta var. californica, and P. muricata. The distribution of A. phalloides is largely within the distribution of its most frequent host, Q. agrifolia. See Supplementary Table S4 for statistics.