Mitochondrial activity in gametes and uniparental inheritance: a comment on 'What can we infer about the origin of sex in early eukaryotes?'

Abstract

In his insightful article, Speijer [1] discussed the origin of sex under multiple points of view, providing a comprehensive and balanced overview of different theories and hypotheses. However, we think that the section ‘Higher mutational loads in one gamete type and retention of uniparental mitochondrial inheritance’ (§9) needs some clarification. Speijer [1] elaborates on the correlation between gamete metabolic and physiological differences and their organellar contribution across generations. Specifically, he quotes the ‘division of labour’ hypothesis, which postulates that male gametes maximize energy production for motility by sacrificing mitochondrial DNA (mtDNA) to oxidative phosphorylation (OXPHOS) and its mutagenic by-products, while non-motile female gametes repress OXPHOS, thus being somewhat inactive [2]. Basically, we clarify two discussion points: (i) the exceptions to the strictly maternal inheritance (SMI) of mitochondria and (ii) the claim that mtDNA is highly mutated in sperm and the supposed causal relationship between such damage and OXPHOS. Exceptions to SMI by which bioenergetically active mitochondria are stably inherited through generations might represent a challenge for the division of labour hypothesis. Doubly uniparental inheritance (DUI) is the only known evolutionarily stable exception to the SMI typical of Metazoa. In DUI animals (approx. 100 species of gonochoric bivalve molluscs identified so far [3]), two mitochondrial lineages are inherited, one through eggs (F-type) and the other through sperm (M-type). Eggs are homoplasmic for the F-type, while spermatozoa are homoplasmic for the M-type. These ‘mother-to-daughter’ and ‘father-to-son’ mitochondrial lineages have evolved independently for millions of years (e.g. more than 200 Myr in unionids), accumulating up to 40% of DNA sequence divergence. Since eggs do not transmit the M-type, germ line mitochondria of DUI males are apportioned from the four/five mitochondria of the fertilizing spermatozoon, which carry mtDNA that must be functional and successfully inherited [ …