A model for the evolution of myco-heterotrophic plants in which speciation of plant lineages and simultaneous specialization of plants to fungi leads to phylogenetic tracking (Merckx and Bidartondo, 2008). (A) A community of generalist mycorrhizal mutualists. Black squares represent mycorrhizal plants in two distant lineages, ((a,b),c) and (w,x). Circles represent mycorrhizal fungi in two distant lineages, ((1,2),3) and ((9,8),7). For instance, 1 and 2 are sister taxa and their closest relative is 3. All plants must be linked to fungi and all fungi must be linked to plants. Double-ended arrows show mutualistic mycorrhizal links where plants provide carbon to fungi and fungi provide mineral nutrients to plants. (B) A mycorrhizal community where plant species x (grey) has lost the ability to photosynthesize so it cannot provide carbon to fungi thereby breaking down the mycorrhizal mutualism. Myco-heterotrophic plants depend on fungi that link them to photosynthetic plants. Single-ended dashed arrows show non-mutualistic mycorrhizal links where fungi provide carbon to plants. Myco-heterotrophic plants have a reduced mycorrhizal range and only associate with related fungi 1, 2 and 3. (C) Speciation of the non-photosynthetic plant lineage x into x′ and x′' leads to further specialixation on fungal lineages; x′ depends on fungus 3 and x′ depends on fungi 1 and 2. The fungi and the photosynthetic plants remain generalist mycorrhizal mutualists. (D) Speciation of plant lineage x′' into y and z. Plant y specializes on fungal host 2 and plant z specializes on closely related fungal host 1. This form of phylogenetic tracking by myco-heterotrophic plants towards pre-existing fungal lineages produces an evolutionary pattern of delayed co-speciation.

Examples of myco-heterotrophic and partially myco-heterotrophic plants from different angiosperm families: (A) Pterospora andromedea, (B) Sarcodes sanguinea (both Pterosporeae; Monotropoideae; Ericaceae), (C) Voyria clavata (Gentianaceae), (D) Cephalanthera damasonium (Orchidaceae), (E) Kupea martinetugei (Triuridaceae), and (F) Afrothismia hydra (Thismiaceae).

Mean δ¹⁵N and δ¹³C values (± s.d.) in leaf tissue of autotrophic, partially myco-heterotrophic and fully myco-heterotrophic plants, as indicated, from two different sites: a beech forest in Germany and a bamboo forest in Japan. Data consolidated from Gebauer and Meyer (2003), Zimmer et al. (2007, 2008) and Ogura-Tsujita et al. (2009). Fully myco-heterotrophic plants are significantly enriched in ¹⁵N and ¹³C compared with autotrophic plants at both sites. The green orchid Cephalanthera damasonium shows similar but slightly less pronounced enrichments in ¹⁵N and ¹³C. At the Bavarian site, Orthilia secunda (Ericaceae) is significantly enriched in ¹⁵N, but not in ¹³C, compared with autotrophic plants. However, at sites where ground-level irradiance is low, a significant myco-heterotrophic gain of ¹³C was detected for this species (Zimmer et al., 2008). Abbreviations: A.pl., Acer platanoides (n = 5); A.ps., Acer pseudoplatanus (n = 9); C.d., Cephalanthera damasonium (n = 5); C.m., Convallaria majalis (n = 12); F.s., Fagus sylvatica (n = 14); G.c., Gastrodia confusa (n = 5); G.p., Gynostemma pentaphyllum (n = 4); M.h., Monotropa hypopitys (n = 4); M.n., Melica nutans (n = 5); N.n., Neottia nidus-avis (n = 14); O.s., Orthilia secunda (n = 5); P.k., Piper kadsura (n = 5); S.a., Sorbus aucuparia (n = 7); T.a., Thelypteris acuminata (n = 5).