Linking paternally inherited mtDNA variants and sperm performance

Abstract

Providing robust links between mitochondrial genotype and phenotype is of major importance given that mitochondrial DNA (mtDNA) variants can affect reproductive success. Because of the strict maternal inheritance (SMI) of mitochondria in animals, haplotypes that negatively affect male fertility can become fixed in populations. This phenomenon is known as ‘mother's curse’. Doubly uniparental inheritance (DUI) of mitochondria is a stable exception in bivalves, which entails two mtDNA lineages that evolve independently and are transmitted separately through oocytes and sperm. This makes the DUI mitochondrial lineages subject to different sex-specific selective sieves during mtDNA evolution, thus DUI is a unique model to evaluate how direct selection on sperm mitochondria could contribute to male reproductive fitness. In this study, we tested the impact of mtDNA variants on sperm performance and bioenergetics in DUI and SMI species. Analyses also involved measures of sperm performance following inhibition of main energy pathways and sperm response to oocyte presence. Compared to SMI, DUI sperm exhibited (i) low speed and linearity, (ii) a strict OXPHOS-dependent strategy of energy production, and (iii) a partial metabolic shift towards fermentation following egg detection. Discussion embraces the adaptive value of mtDNA variation and suggests a link between male-energetic adaptation, fertilization success and paternal mitochondria preservation. This article is part of the theme issue ‘Linking the mitochondrial genotype to phenotype: a complex endeavour’.

An Unusual Evolutionary Strategy: The Origins, Genetic Repertoire, and Implications of Doubly Uniparental Inheritance of Mitochondrial DNA in Bivalves

“…Interestingly, bearing the Mtype mitochondria did not provide any visible advantage in term of speed, with "masculinized" F-type sperm swimming equal or even faster than M-type sperm (Everett et al 2004;Jha et al 2008). Congruent results were recently found by Bettinazzi et al (2020), who extended this investigation to various bivalves with a different mode of mitochondria transmission (i.e. SMI, whose sperm carry the maternal mitochondria, and DUI, whose sperm bear the paternal mitochondria).…”

“…Conversely, sperm of the DUI species M. edulis and R. philippinarum appear to strictly rely on OXPHOS in absence of oocytes, but partially switch towards a more combined strategy, implying also fermentation, once detecting egg-derived chemical cues (Bettinazzi et al 2020).…”

“…During the last decade, several studies have investigated the potential benefits of carrying male-derived mitochondria for bivalve sperm performance (Everett et al 2004;Jha et al 2008;Stewart et al 2012;Bettinazzi et al 2020). Everett et al (2004) and Jha et al (2008) tested this assumption in the DUI species M. edulis, comparing motility traits between "standard" sperm, carrying the M-type mtDNA, and "masculinized" sperm, carrying primarily F-type mtDNA with a segment of M-type control region sequence (called RM-types).…”

“…SMI, whose sperm carry the maternal mitochondria, and DUI, whose sperm bear the paternal mitochondria). In sharp contrast with sperm carrying maternally inherited mitochondria (SMI system), M-type sperm of the DUI species M. edulis and R. philippinarum exhibit a convergent readapted phenotype, characterized by lower speed and accentuate curvilinear trajectory (Bettinazzi et al 2020). Differences in sperm performance also reflect change in the energetic strategy that fuels sperm motility.…”

Faraway, so close. The comparative method and the potential of non-model animals in mitochondrial research

“…Because of SMI, some authors predict that mitochondrial quality control is less effective in males ('Mother's curse hypothesis', see [44,45]). Bettinazzi et al [35] use the only known evolutionarily stable exception to SMI to investigate the link between mtDNA variants and sperm performance. Because of the strict maternal inheritance of mitochondria in animals, haplotypes that negatively affect male fertility can become fixed in populations.…”