Selection for male-enforced uniparental cytoplasmic inheritance

Abstract

In most sexually reproducing species, including humans, mitochondria and other cytoplasmic elements are uniparentally (usually maternally) inherited. This phenomenon is of broad interest as a mechanism for countering the proliferation of selfish mitochondria. Uniparental inheritance can be enforced either by the female gametes excluding male cytoplasm or male gametes excluding their own from the zygote. Previous studies have shown that male-enforced uniparental inheritance is unlikely to evolve as a primary mechanism, because unlike female enforcement, the positive linkage disequilibrium between the modifier for eliminating the gamete’s own mitochondria and a wild-type mitochondrial complement is broken from one generation to the next. However, it has been proposed that with a sufficiently high mutation rate and strong selection, elimination of the gamete’s own mitochondria could be favored by selection. In this article, a series of numerical simulations confirm that this is indeed the case, although the conditions where male enforcement is favored are quite restrictive. Specifically, in addition to a high mutation rate to selfish mitochondria and strong selection against them, the cost of uniparental inheritance must be negligible.