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

Abstract

The fields of evolutionary biology, molecular ecology, genetics, and taxonomy have been profoundly influenced by studies of variation in mitochondrial DNA (mtDNA), yet there are often surprising differences between mtDNA and nuclear DNA in the within- and between-population relationships that they display. Here I articulate and evaluate a hypothesis that may explain many of the cases in which mtDNA shows little within-population variation and recent movement between populations. Many taxonomic groups (e.g., birds, butterflies and moths; most snakes; some amphibians, fish, and plants) have sex chromosome systems in which females are heterogametic (i.e., ZW females and ZZ males). If a W chromosome undergoes a mutation that gives it a transmission advantage in getting into the one egg produced by female meiosis, it will tend to cause a female-biased sex ratio in the offspring of females that carry that driving W chromosome. This sex ratio bias increases the frequency of the driving W in relation to the non-driving W in the next generation. In the great majority of species in which mitochondria are inherited matrilineally, the spread of the driving W through the population will carry along the particular mitochondrial genome that happens to be associated with the driving W. I summarize evidence in support of the seven components of this W-mtDNA Drive Hypothesis and present simulations and mathematical formulae showing that W drivers spread much more rapidly than equivalent-strength Z or autosomal drivers. Suppressors of W drive spread at a vastly lower rate. I conclude that many cases of low within-population mitochondrial diversity and mitochondrial transfer between species might be explained by the spread of driving W chromosomes.