The risk of sexual reproduction promotes the evolution of regulation between host and symbionts

Abstract Sexual reproduction is a widely spread feature of eukaryotes and was already present in the last eukaryotic common ancestor. While most extant eukaryotes inherit mitochondria from a single parent, the mechanisms enforcing uniparental inheritance vary widely. The first eukaryotes likely would not have evolved such mechanisms yet, so cellular fusion would have led to mitochondrial mixing (biparental inheritance). Here, we explore the evolutionary consequences of biparental inheritance of endosymbionts during host–symbiont coevolution using a multi-level, individual-based model of endosymbiosis. Our results show that biparental inheritance introduces evolutionary conflict, as it facilitates the spread of fast-replicating symbionts, which can drive host populations to extinction. However, in a diverse environment, proto-eukaryotes diversify and adapt to distinct niches, protecting the population from total collapse caused by selfish symbionts. Moreover, this conflict can be resolved through the evolution of signalling mechanisms that allow hosts to regulate symbiont cell cycles. In many cases, sexually reproducing populations not only survive but also outperform their asexual counterparts. We conclude that sexual reproduction could have appeared early during eukaryogenesis and may have facilitated the evolution of host control over the endosymbiont cell cycle. This article is part of the theme issue ‘Evolutionary genetics of mitochondria: on diverse and common evolutionary constraints across eukarya’.