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Background  Mycorrhizal fungi form intimate associations with their host plants that constitute their carbon resource and habitat.  Alnus  spp. (Betulaceae) are known to host an exceptional species-poor and specialized ectomycorrhizal (ECM) fungal community compared to other tree species, but the host-specificity pattern and its significance in terms of fungal diversification and speciation remain poorly documented. The degree of parallel speciation, host switching, and patterns of biogeography were explored in the historical associations between alders and three ECM taxa of Basidiomycetes:  Alnicola  (Agaricales),  Alpova  (Boletales), and  Lactarius  (Russulales). The aim was to develop an evolutionary framework on host specificity and diversification of Basidiomycetes in this highly specialized plant-fungus symbiosis.    Results  Sporocarps of  Alnicola  (220),  Lactarius  (61) and  Alpova  (29) were collected from stands of the four European alder species ( A. alnobetula  including the endemic subsp.  suaveolens  in Corsica,  A. cordata ,  A. glutinosa ,  A. incana ) in Western Europe (mainly in France and Austria), from 1995 to 2009. Specimens were morphologically identified to the species level. From these, 402 sequences of four DNA regions (ITS, rpb2, gpd, and the V9 domain of the mit-SSU rDNA) were successfully obtained and analyzed in addition with 89 sequences available in GenBank and UNITE databases. Phylogenetic analyses were conducted on all sequence data sets (individual and combined) using maximum likelihood reconstruction and Bayesian inference. Fungal phylogenies are compared and discussed in relation to the host, with a focus on species boundaries by associating taxonomic, systematic and molecular information.    Conclusions  Patterns of host specificity and phylogenies of  Alnicola  and  Lactarius  suggest coevolution as a basal factor of speciation in relation with the subgeneric diversification of  Alnus , possibly due to the very selective pressure of the host. A second element of the historical associations between  Alnus  and its fungal symbionts is a host-dependent speciation (radiation without host change), here observed in  Alnicola  and  Alpova  in relation with  Alnus  subgen.  Alnus . Finally host shifts from  Alnus  subgen.  Alnus  to  A. alnobetula  are found in most lineages of  Alnicola  (at least four times),  Alpova  (twice) and  Lactarius  (once), but they do not represent such a common event as could be expected by geographic proximity of trees from the two subgenera. However, active or very recent host extensions clearly occurred in Corsica, where some fungi usually associated with  Alnus glutinosa  on mainland Europe locally extend there to  A. alnobetula  subsp.  suaveolens  without significant genetic or morphological deviation.

Comparative phylogenies and host specialization in the alder ectomycorrhizal fungi Alnicola, Alpova and Lactarius (Basidiomycota) in Europe