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Host islands within the California Northern Channel Islands

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Molecular Ecology (2007) doi: 10.1111/j.1365-294X.2007.03264.x© 2007 The AuthorsJournal compilation © 2007 Blackwell Publishing Ltd Blackwell Publishing Ltd Host islands within the California Northern Channel Islands create fine-scale genetic structure in two sympatric species of the symbiotic ectomycorrhizal fungus Rhizopogon LISA C. GRUBISHA, * SARAH E. BERGEMANN † and THOMAS D. BRUNS * * Department of Plant and Microbial Biology, 111 Koshland, University of California, Berkeley, CA 94720-3102, USA, † Department of Environmental Science, Policy and Management, Ecosystem Science Division, 137 Mulford Hall, University of California, Berkeley, CA 94720, USA AbstractWe have examined fine-scale genetic structure of the symbiotic ectomycorrhizal fungi Rhizopogon occidentalis and R. vulgaris on two of the California Channel Islands usingfive and six microsatellite loci, respectively. Both Rhizopogon species are sympatric on SantaCruz and Santa Rosa Islands and are ectomycorrhizal with bishop pine ( Pinus muricata ) onboth islands or Santa Rosa Island Torrey pine ( P. torreyana ssp. insularis ) on Santa Rosa.The combination of disjunct pine host distributions and geographic barriers within andamong the islands have created highly structured Rhizopogon populations over very shortdistances (8.5 km on Santa Cruz Island; F ST = 0.258, F ST = 0.056, R. occidentalis and R. vulgaris ,respectively). Both species show similar patterns of genetic differentiation as a result oflimited dispersal between host populations as revealed by a significant isolation by distancerelationship ( r = 0.69, P < 0.04; r = 0.93, P < 0.001, R. occidentalis and R. vulgaris , respectively)and Bayesian clustering analyses, and is most likely a function of the small foraging rangeof the few mammals that disperse Rhizopogon on these islands and the enormous sporebank characteristic of Rhizopogon species. Keywords : animal dispersal, genetic distance, hypogeous fungi, microsatellite loci, phylogeography,spore banks Received 9 September 2006; revision accepted 4 December 2006 Introduction Islands are considered to be natural laboratories forevolution (Darwin 1859; Mayr 1963). Founding events aretypically believed to involve few individuals or propagules(Mayr 1942; Whittaker 1998) and thus random genetic driftand selection may result in rapid evolution (Barton 1998).Insular populations are likely to have less genetic diver-sity within populations and greater genetic divergencebetween populations (Nei et al . 1975; Chakraborty & Nei1977; reviewed by Frankham 1997).Ectomycorrhizal fungi form obligate, symbiotic interac-tions with roots of many forest trees. This mutualisminvolves the exchange of mineral nutrients that the fungiobtain from the soil for photosynthetically fixed carbon,produced by the plants (Smith & Read 1997). The obligatenature of the interaction means that ectomycorrhizal fungiare restricted to habitats that contain appropriate hostplants. When host populations are discrete and isolated,such ‘host islands’ have the potential to affect the structureof fungal populations, particularly in cases where dispersalof the fungus is relatively limited and thus functions as amosaic of isolated subpopulations. Furthermore, isolatedhost islands within real islands provide an opportunity toexamine the factors causing geographic variation comparedto strictly inter-island or island–mainland studies (Thorpe& Malhotra 1998). Rhizopogon species (Basidiomycota, Boletales) might beexpected to be particularly prone to the host island effect Correspondence: L. C. Grubisha, Fax: (1) (907) 474-6967; E-mail:[email protected]‡Present address: Institute of Arctic Biology, 311 Irving I Building,902 N. Koyukuk Drive, University of Alaska, Fairbanks, AK99775-7000, USA2 L. C. GRUBISHA, S. E. BERGEMANN and T. D. BRUNS © 2007 The AuthorsJournal compilation © 2007 Blackwell Publishing Ltd because they tend to have narrow host ranges and theirspores are animal dispersed. Rhizopogon is symbiotic almostexclusively with members of the Pinaceae and species areoften restricted to Pinus or Pseudotsuga species (Molina et al . 1999). In many ecosystems this means that individual Rhizopogon species are effectively restricted to a single hostspecies. Rhizopogon produces meiotic spores in below-ground, ‘hypogeous’ sporocarps, called false-truffles. Thesesporocarps are dispersed primarily by small rodents,and less frequently by larger mammals (Maser et al . 1978;Currah et al . 2000; Ashkannejhad & Horton 2006). Thedispersal of Rhizopogon is limited by the foraging range ofmammal vectors compared to above-ground ‘epigeous’mushroom-forming fungi that have the potential to havewindborne spore dispersal.Local populations of Rhizopogon are likely to be large andpersistent through time because they form extensive soilspore banks, analogous to seed banks in plants. Spores aredeposited in soil when Rhizopogon false-truffles that are notconsumed by mammals deliquesce in place or whendispersed spores are deposited by mammal fecal pellets(Miller et al . 1994). Within pine forests these spore banksare so dense that even when soils are diluted 50 to 100-foldinto sterile soil more that half of the test seedlings plantedwill still be colonized by Rhizopogon species (Taylor &Bruns 1999; Kjøller & Bruns 2003; Rusca et al . 2006). Wenow estimate that this translates to at least 3000 Rhizopogon spore/mL of soil for an average pine forest in California(TD Bruns, unpublished). The longevity of these sporebanks is not known, but some observations suggest thatthey may last at least for decades (Izzo et al . 2005). Thus, wewould anticipate that Rhizopogon spore banks have increasedover time, and that rare migration events would likely beundetected without the selective sweep of advantageousalleles from migrant individuals and hitchhiking by neutralmicrosatellite loci.In the present study our primary goal was to examinethe fine-scale population structure, based on microsatelliteloci, of Rhizopogon occidentalis and R. vulgaris, two pine-associated Rhizopogon species, in a setting where popula-tions appeared to be separated into localized host islandson the scale of a few kilometers. We hypothesized that wewould find significant genetic structure in such a setting, dueto the dispersal, host and population biology of Rhizopogon discussed above. We were able to use two


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