Cheating in arbuscular mycorrhizal mutualism: a network and phylogenetic analysis of mycoheterotrophy

Abstract

Although mutualistic interactions are widespread and essential in ecosystem functioning, the emergence of uncooperative cheaters threatens their stability, unless there are some physiological or ecological mechanisms limiting interactions with cheaters.In this framework, we investigated the patterns of specialization and phylogenetic distribution of mycoheterotrophic cheaters vs noncheating autotrophic plants and their respective fungi, in a global arbuscular mycorrhizal network with> 25 000 interactions.We show that mycoheterotrophy evolved repeatedly among vascular plants, suggesting low phylogenetic constraints for plants. However, mycoheterotrophic plants are significantly more specialized than autotrophic plants, and they tend to be associated with specialized and closely related fungi. These results raise new hypotheses about the mechanisms (e.g. sanctions, or habitat filtering) that actually limit the interaction of mycoheterotrophic plants and their associated fungi with the rest of the autotrophic plants.Beyond mycorrhizal symbiosis, this unprecedented comparison of mycoheterotrophic vs autotrophic plants provides a network and phylogenetic framework to assess the presence of constraints upon cheating emergences in mutualisms.

Specificity of assemblage, not fungal partner species, explains mycorrhizal partnerships of mycoheterotrophic Burmannia plants

“…Investigation of the strength and importance of partner selection between MHPs and AMF under natural settings represents an invaluable contribution to studies of mycorrhizal ecology [10]. MHPs are either specialized on single fungal families, genera, or-in extreme casesspecies [11], and are generally more specific to AMF than that of autotrophic plants [2,[11][12][13][14][15], although the degree of specificity varies by species and across families, some MHPs such as Thismia exhibit extremely high fungal specificity [14,16], whereas other taxa interact simultaneously with a wide range of AMF lineages [17,18]. These studies suggest that different MHP groups likely have divergent interaction patterns toward mycorrhizal fungi.…”

Mycorrhizal fungi control phosphorus value in trade symbiosis with host roots when exposed to abrupt ‘crashes’ and ‘booms’ of resource availability

“…Although the principles of biological market theory are generally well supported in mycorrhizal studies, there are also well documented examples of resource exchange between plants and fungi that do not follow market theory predictions (Olsson et al ., 2010; Walder et al ., 2012; Walder & van der Heijden, 2015; Field & Pressel, 2018; Charters et al ., 2020). Some of these examples, including elegant work on mycoheterotrophic plant species (Bidartondo, 2005; Courty et al ., 2011; Gomes et al ., 2019; Perez‐Lamarque et al ., 2020), are clear illustrations of how reciprocal exchange patterns can be violated depending on context. While neither the disappearance of cheating nor perfect partner choice is predicted by biological market theory (Kiers et al ., 2016; Noë & Kiers, 2018), many open questions remain on the mechanisms that underlie recipiorocal exchange patterns.…”

Global drivers of obligate mycorrhizal symbionts diversification

“…or sampled directly from soil, we only retained the sequences of AMF that occurred in natural ecosystems and interacted with a plant identified at the species level 12 (dataset 2, Supplementary Table 7). This filtering led to 351 fungal VT interacting with a total of 490 plant species 24 . For each VT or EU "species" containing at least 10 sequences in dataset 2, we computed genetic diversity using Tajima's estimator (θπ) 69 , which corresponds to the mean pairwise differences between sequences, while accounting for the nucleotide gaps frequent in such metabarcoding datasets (Supplementary Materials 1) 91 .…”

“…For the plants, we used the Plant List (http://www.theplantlist.org) to update some taxonomic assignations following the Angiosperm Phylogeny Group (APG) III system. The land plant phylogenetic tree of the 490 species was obtained by pruning the synthesis phylogeny 27 using Phylomatic (http://phylodiversity.net/phylomatic/) and manually grafting the 37 missing taxa onto the Phylomatic tree as polytomies based on the current literature 24 .…”

“…Other abiotic factors include habitat: tropical grasslands have, for example, been suggested as diversification hotspots for AMF [25]. Besides abiotic factors, AMF are obligate symbionts and, although relatively generalist [4, 26, 27], their evolutionary history could be largely influenced by a diffuse coevolution with their host plants [10, 28, 29]. Over the last 400 Myr, land plants have experienced massive extinctions and radiations [29, 30], adaptations to various ecosystems [31, 32], and associations with different soil microorganisms [33, 34].…”