Relative strength of fine-scale spatial genetic structure in paternally vs biparentally inherited DNA in a dioecious plant depends on both sex proportions and pollen-to-seed dispersal ratio

Abstract

In plants, the spatial genetic structure (SGS) is shaped mainly by gene dispersal and effective population density. Among additional factors, the mode of DNA inheritance and dioecy influence SGS. However, their joint impact on SGS remains unclear, especially in the case of paternally inherited DNA. Using theoretical approximations and computer simulations, here we showed that the relative intensity of SGS measured in paternally and biparentally inherited DNA in a dioecious plant population depends on both the proportion of males and the pollen-to-seed dispersal ratio. As long as males do not prevail in a population, SGS is more intense in paternally than biparentally inherited DNA. When males prevail, the intensity of SGS in paternally vs biparentally inherited DNA depends on the compound effect of sex proportions and the pollen-to-seed dispersal ratio. To empirically validate our predictions, we used the case of Taxus baccata, a dioecious European tree. First, we showed that mitochondrial DNA (mtDNA) in T. baccata is predominantly (98%) paternally inherited. Subsequently, using nuclear DNA (nuDNA) and mitochondrial microsatellite data, we compared the fine-scale SGS intensity at both marker types in two natural populations. The population with equal sex proportions showed stronger SGS in mtDNA than in nuDNA. On the other hand, we found lower SGS intensity in mtDNA than in nuDNA in the population with 67% males. Thus, the empirical results provided good support for the theoretical predictions, suggesting that knowledge about SGS in paternally vs biparentally inherited DNA may provide insight into effective sex proportions within dioecious populations.