Life history costs drive the evolution of mycoheterotrophs: Increased sprouting and flowering in a strongly mycoheterotrophic Pyrola species

Abstract Land plants are typically photosynthetic, but some species have lost the ability to photosynthesize, instead relying on mycorrhizal fungi to obtain carbon. Increasing levels of partial mycoheterotrophy, in which seemingly autotrophic plants receive fungal carbon from their fungal partners, and reduced sprouting in concert with greater reproduction when sprouting, may be intermediate steps in the evolution of this trait. We studied the microevolutionary demography of Pyrola japonica and the closely related species P. subaphylla, which are currently considered sister species. While these species are both partially mycoheterotrophic, P. subaphylla is more strongly so, indicating that it may be closer to evolving full mycoheterotrophy. We tracked individuals in two nearby populations in Fukushima, Japan from 2015 to 2020. We analysed vital rates, population trends and long‐run population structure with historical function‐based matrix projection models. We assessed how shifts in P. subaphylla demography relate to fitness using a stochastic life table response experiment (SLTRE). P. subaphylla exhibited strong costs of growth to survival and of reproduction to sprouting, size and fecundity. It sprouted more than P. japonica but to smaller stages. P. subaphylla's flowering frequency was approximately four times that of P. japonica, but after flowering it was smaller and more likely to die. These life history costs appeared to drive differences in fitness, measured as stochastic population growth rate. Relative to P. japonica, shifts in fitness in P. subaphylla were due more to shifts in means than standard deviations of matrix elements. Shifts in growth transitions had the strongest negative impacts on fitness but also had the strongest positive impacts. Increased shifts to small non‐flowering stages were associated with increased fitness, while transitions involving dormancy were associated more strongly with drops in fitness. Synthesis. As far as we are aware, we found the first evidence that costs of growth and reproduction drive the evolution of increased sprouting and smaller size as a species becomes more intensely mycoheterotrophic. Surprisingly, vegetative dormancy did not evolve with mycoheterotrophy. We suggest further studies assessing whether these seemingly maladaptive trends result from genetic drift, genetic linkage or another mechanism.