The evolutionary ecology of myco‐heterotrophy

Abstract

Contents Summary 1 Introduction 1 Monotropa: over 180 years of controversy 3 Do all epiparasites evolve from photosynthetic mycorrhizal ancestors? 5 What is unique about the monotrope radiation? 8 Potential sources of exceptional myco‐heterotrophy 10 What form of carbon moves from fungus to plant? 10 Mycorrhizas vs reproduction? 11 What fungal signal triggers symbiotic seed germination? 12 Conclusions 14 Acknowledgements 14 References 14 Summary Nonphotosynthetic mycorrhizal plants have long attracted the curiosity of botanists and mycologists, and they have been a target for unabated controversy and speculation. In fact, these puzzling plants dominated the very beginnings of the field of mycorrhizal biology. However, only recently has the mycorrhizal biology of this diverse group of plants begun to be systematically unravelled, largely following a landmark Tansley review a decade ago and crucial developments in the field of molecular ecology. Here I explore our knowledge of these evolutionarily and ecologically diverse plant–fungal symbioses, highlighting areas where there has been significant progress. The focus is on what is arguably the best understood example, the monotropoid mycorrhizal symbiosis, and the overarching goal is to lay out the questions that remain to be answered about the biology of myco‐heterotrophy and epiparasitism.

Evidence of a myco-heterotroph in the plant family Ericaceae that lacks mycorrhizal specificity

“…Fungal endophytes in the genus Phialocephala and the order Helotiales, which may contain some EM species (Vrålstad et al 2002), also appear to be common associates of Pyroleae, though their functional role within the plant roots is unclear. Pyroloids also associate with EM fungal genera and species such as Russula (Zimmer et al 2007;Vincenot et al 2008 and this study), Tricholoma (Tedersoo et al 2007;Vincenot et al 2008) and Rhizopogon salebrosus (this study) that are known to form mycorrhizas with other ericaceous myco-heterotrophs (Bidartondo 2005).…”

“…This tripartite interaction between a myco-heterotrophic plant, an autotrophic plant and a shared mycorrhizal fungus is an epiparasitism where the potential fitness costs to the fungus are still unknown (Bidartondo 2005). All mycoheterotrophic epiparasitisms are thought to have evolved from initial tripartite associations between two autotrophic plants sharing at least one mycorrhizal fungus (Bidartondo 2005). However, the ordering of the steps that lead to one plant defaulting on the mycorrhizal mutualism remains the subject of debate.…”

“…In the latter group, there are some species that act as carbon sinks and gain carbon via mycorrhizal fungi that they share with surrounding autotrophic plants. This tripartite interaction between a myco-heterotrophic plant, an autotrophic plant and a shared mycorrhizal fungus is an epiparasitism where the potential fitness costs to the fungus are still unknown (Bidartondo 2005). All mycoheterotrophic epiparasitisms are thought to have evolved from initial tripartite associations between two autotrophic plants sharing at least one mycorrhizal fungus (Bidartondo 2005).…”

The Coexistence of Hosts with Different Abilities to Discriminate against Cheater Partners: An Evolutionary Game-Theory Approach

“…Consistent with this finding, several generalist mycorrhizal species have evolved to exploit plant C without providing any benefits (Graham and Abbott 2000;Burleigh et al 2002;Smith et al 2003Smith et al , 2004Koch et al 2006;Violi et al 2007). In contrast, although plants provide up to 20% of their fixed C to their mycorrhizal partners, the benefits of acquiring limiting soil P can result in a net increase in photosynthetic rate that more than defrays this cost (Kaschuk et al 2009), such that plant cheaters appear to be restricted to highly specialized mycoheterophic species that specialize in low-light environments in the forest understory (Bidartondo 2005). In this context, allocating C to mycorrhizal fungi is costly only if the fungal partner fails to offset this investment with a sufficient augmentation of host photosynthetic rate; that is, when a plant associates with cheater fungi (with cost K).…”

Comparative Dating of Attine Ant and Lepiotaceous Cultivar Phylogenies Reveals Coevolutionary Synchrony and Discord

“…However, most mutualistic symbioses involve complex patterns of interactions among multiple species pools rather than pairwise specialization (Borowicz and Juliano 1991;Bruns et al 2002;Clay and Schardl 2002;Thompson 2005;Ollerton 2006;Herre et al 2008). Less intimate symbioses characterized by host sharing or symbiont switching frequently produce intricate patterns of complete or partial discord between symbiont phylogenies (e.g., termites and their fungal cultivars [Aanen et al 2002], figs and fig wasps [Machado et al 2005;Herre et al 2008;Jackson et al 2008], yucca moths and yucca [Smith et al 2008], squid and their bioluminescent symbionts [Dunlap et al 2007], lichen symbioses [Piercey-Normore and DePriest 2001;Rikkinen et al 2002], and mycorrhizal symbioses [Bidartondo 2005;Shefferson et al 2007]). A major goal of current efforts is to understand the coevolutionary dynamics of complex mutualistic interactions (Ollerton 2006;Guimarães et al 2007;Jousselin et al 2008).…”