The optimal mating distance resulting from heterosis and genetic incompatibility

Theory predicts that the fitness of an individual is maximized when the genetic distance between its parents (i.e., mating distance) is neither too small nor too large. However, decades of research have generally failed to validate this prediction or identify the optimal mating distance (OMD). Respectively analyzing large numbers of crosses of fungal, plant, and animal model organisms, we indeed find the hybrid phenotypic value a humped quadratic polynomial function of the mating distance for the vast majority of fitness-related traits examined, with different traits of the same species exhibiting similar OMDs. OMDs are generally slightly greater than the nucleotide diversities of the species concerned but smaller than the observed maximal intraspecific genetic distances. Hence, the benefit of heterosis is at least partially offset by the harm of genetic incompatibility even within species. These results have multiple theoretical and practical implications for speciation, conservation, and agriculture.