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

Sexual reproduction is a widely spread feature of eukaryotes and was already present in the last eukaryotic common ancestor (LECA). Most extant eukaryotes inherit mitochondria from a single parent, but the mechanisms enforcing uniparental inheritance vary widely. Yet, because the first eukaryotes would not have evolved such mechanisms, sexual cell fusion would have inherently led to mitochondrial mixing. Here, we explore the evolutionary consequences of biparental inheritance of endosymbionts during host–symbiont co-evolution using a multilevel, 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, holobionts 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 signaling 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.