Abstract: Plants are typically, but many have lost the ability to photosynthesize in exchange for mycoheterotrophy, in which mycorrhizal fungi are the dominant carbon source for the plant. While the macroevolution of this transition has been studied recently, particularly in orchids, the microevolutionary path toward the loss of photosynthesis remains a mystery. We studied the microevolution of loss of photosynthesis and gain of mycoheterotrophy with a demographic study of the predominantly photosynthetic species Pyrola japonica, and its close relative P. subaphylla. While the latter species is not non-photosynthetic, it has been identified and much more strongly mycoheterotrophic than P. japonica. We tracked individuals in nearby populations of these two species near Mt. Bandai, Japan from 2015 to 2020. We analyzed demographic trends in both populations, particularly through the creation of historical function-based matrix projection models (fbMPMs) parameterized with vital rate models developed for each population with R package lefko3. We compared these trends relative to the stochastic growth rate using the small-noise approximation life table response experiment (SNA-LTRE), in which P. japonica was used as a reference population to compare trends in P. subaphylla. Both populations decreased throughout the course of the study. Trends in P. subaphylla primarily differed from P. japonica via shifts in mean element values. Particularly, shrinkage transitions had strong impacts on the population growth rate, while differences in fecundity had minimal impact. P. subaphylla was more likely to sprout and flower than P. japonica, and these differences had a more positive impact on the population growth rate. However, P. japonica grew larger and exhibited higher survival. Our results suggest that the evolution of mycoheterotrophy may be associated generally with drops in survival but increased tendency toward flowering when individuals do sprout. Such a trade-off has been observed before in some orchids, and now for the first time in the Ericaceae.
