Coevolution describes evolutionary change in which two or more interacting species reciprocally drive each other’s evolution. Much progress has been made in analyzing its dynamics and consequences, but little is understood about how coevolutionary selection operates within multispecies interactions, i.e., those with diverse suites of species on one or both sides of an interaction. We investigated natural selection on pine and ectomycorrhizal fungi (ECM) fungal traits, including candidate coevolving traits that govern interactions between pines and ECM fungi. Using genotypes of Monterey pine (Pinus radiata) from isolated populations along the west coast of California (USA) and Baja California (Mexico), we performed a common garden experiment at one of those populations on mainland California (Cambria). We planted 1178 seedling genotypes from all five native populations of Monterey Pine, as well as crosses to represent intermediate phenotypes/genotypes, for a total of 47 unique genetic families. We then measured pine seedling traits, ECM fungal traits, and ECM species composition and related them to relativized measures of plant and fungal fitness using standard procedures for calculating selection gradients. Coevolutionary selection was assessed using interaction terms combining plant and fungal traits.
Results/Conclusions
We found evidence for natural selection on a variety of plant and ECM traits, including potential coevolutionary selection for several pairs of traits. Specifically, the fungal trait fungal hyphal biomass, which separated low biomass from high biomass fungi, played a significant role in coevolutionary selection for the plant traits relative growth rate (RGR) and specific root length (SRL), although the nature of selection varied depending on whether plant or fungal fitness was evaluated. In fungal fitness models, selection was positive, experiencing peak selection across multiple combinations of RGR / SRL values but declining to a single value; in plant fitness models, selection was negative, stemming from a single peak fitness value and declining across multiple combinations of RGR / SRL. Patterns of coevolutionary selection for plant diameter were similar for fungi with a range of fungal traits relating to their ability to extract nutrients from the soil (long distance, medium distance smooth, short distance, contact), with a single relative fitness peak and decreasing fitness from this peak. This work represents the first field-based, community-level investigation of coevolutionary selection in a multispecies nutritional symbiosis, suggesting that ongoing coevolution and interspecific selection are important contemporary forces driving trait evolution in these interactions.