The Driving W Hypothesis for Low Within-Population Mitochondrial DNA Diversity and Between-Population Mitochondrial Capture

The fields of evolutionary biology, molecular ecology, genetics, and taxonomy have been profoundly influenced by studies of variation in mitochondrial DNA. Here I propose a hypothesis that will likely contribute to a full understanding of commonly observed differences in patterns of variation in mitochondrial DNA versus phenotypic traits and nuclear autosomal DNA. The Driving W Hypothesis applies to the many taxonomic groups (e.g., birds, butterflies and moths; most snakes; some amphibians, fish, and plants) in which females are heterogametic (i.e., have ZW sex chromosomes). If a W chromosome undergoes a mutation that gives it a transmission advantage in getting into the one egg produced by female meiosis, the driving W chromosome can spread rapidly through a population, carrying along the particular mitochondrial genome that happens to be associated with the driving W. Simulations show that W drivers spread much more rapidly than equivalent-strength Z or autosomal drivers, and that autosomal suppressors of W drive spread at a vastly lower rate. I summarize the logic and evidence in support of the seven components of this hypothesis and conclude that the driving W hypothesis has tremendous potential to explain observations of low within-population mitochondrial diversity as well as cases of "mitochondrial capture" between species.