Mutualism Persistence and Abandonment during the Evolution of the Mycorrhizal Symbiosis

Mutualistic symbioses with mycorrhizal fungi are widespread in plants. The majority of plant species associate with arbuscular mycorrhizal (AM) fungi. By contrast, the minority associate with ectomycorrhizal (EM) fungi, have abandoned the symbiosis and are nonmycorrhizal (NM), or engage in an intermediate, weakly AM symbiosis (AMNM). To understand the processes that maintain the mycorrhizal symbiosis or cause its loss, we reconstructed its evolution using a ∼3,000-species seed plant phylogeny integrated with mycorrhizal state information. Reconstruction indicated that the common ancestor of seed plants most likely associated with AM fungi and that the EM, NM, and AMNM states descended from the AM state. Direct transitions from the AM state to the EM and NM states were infrequent and generally irreversible, implying that natural selection or genetic constraint could promote stasis once a particular state evolved. However, the evolution of the NM state was more frequent via an indirect pathway through the AMNM state, suggesting that weakening of the AM symbiosis is a necessary precursor to mutualism abandonment. Nevertheless, reversions from the AMNM state back to the AM state were an order of magnitude more likely than transitions to the NM state, suggesting that natural selection favors the AM symbiosis over mutualism abandonment.