Mycorrhizal arbitrage, a hypothesis: How mycoheterotrophs could profit from inefficiencies in the biological marketplace

Abstract

Mycoheterotrophy, whereby plants acquire both carbon and nutrients from a fungal partner, is an evolutionarily puzzling phenomenon. According to biological market models, mycoheterotrophs have nothing to offer and thus should be shunned as trading partners by discriminating fungi. Nevertheless, mycoheterotrophy is common, particularly among orchids, and an estimated 10% of all plant species are facultatively mycoheterotrophic at early stages in their life cycle. Reconciling mycoheterotrophy with biological market models, I describe how mycoheterotrophs could use arbitrage trading to net a profit of carbon and nutrients, without acquiring either from the abiotic environment. The model requires that mycoheterotrophs simultaneously buy and sell both carbon and nutrients, exploiting variability in the trading ratios offered by mycorrhizal fungi. The model relies on several conditions, including the ability of the mycoheterotroph to form indirect hyphal associations with two or more neighbouring autotrophic mycorrhizal associations, the existence of variable carbon:nutrient exchange ratios among these associations and the ability of mycoheterotrophs to invert the net-direction of resource trade. Evidence that these conditions occur in a state of nature varies from incontrovertible to plausible given available models. The arbitrage model provides evolutionary rationale for mycoheterotrophy from both the plant and fungal perspective. Accordingly, mycoheterotrophs match trading ratios offered by autotrophic plants and, thus, need not be antagonists. The model makes novel predictions that distinguish it from source-sink models, most notably in the existence of resource exchange inversions at the plant-mycorrhizal interface. Finally, the model emphasizes market inefficiencies as the foundation on which mycoheterotrophs construct an arbitrage niche. Read the free Plain Language Summary for this article on the Journal blog.