Demographic shifts related to mycoheterotrophy and their fitness impacts in two Cephalanthera species

Evolutionary losses of photosynthesis in terrestrial plants all originate in photosynthetic ancestors. The adaptive context under which this transition happens has remained elusive because of the rarity of plants in which both photosynthetic and non-photosynthetic forms exist as a polymorphism. Here, we report on demographic patterns in photosynthetic ("green") and nonphotosynthetic ("albino") individuals within populations of two such species, Cephalanthera damasonium and C. longifolia, which also acquire nutrition from their mycorrhizal hosts (partial mycoheterotrophy). We hypothesized that demographic shifts in albinos relative to greens would include compensatory patterns with respect to fitness, such that maladaptive changes to survival or reproduction would be adaptively countered by changes to other parameters, such as growth probabilities. We tracked individuals in two populations of C. damasonium for 3 yr, and in one population of C. longifolia for 14 yr. We then analyzed vital rates for both phenotypes using general linear mixed models (GLMMs) and multi-state capture mark-recapture models (CMR), and used these models to develop size-classified, function-based population projection matrices. We estimated fitness as the deterministic population growth rate (λ) for each phenotype, and explored the impact of shifts in demographic patterns to albinism via life table response experiments (LTREs). Mortality differed between greens and albinos, but not similarly across species. Albinos generally sprouted less than greens, and flowered more when small but less at other times. Albinos typically had a higher probability of fruiting, although their lower flower numbers yielded lower numbers of fruits overall. Fitness did not differ significantly among phenotypes. Thus, we did not find significant evidence that albinism is adaptive or maladaptive; however, if in fact it is the latter, then we did find evidence of incomplete compensation for declines in survival and reproduction from growth transitions, particularly to small flowering size classes in C. damasonium, and to large vegetative size classes in C. longifolia. These patterns indicate some support for the idea that albinism may lead to the speciation of mycoheterotrophic plants.