Beneficial microbes may have favoured the evolution of adaptive immunity

Vertebrate adaptive immunity has long been considered uniquely advantageous for its capacity to recognise and remember a wide diversity of molecular targets, potentially conferring lasting defence from any threatening microbe. However, over the last two decades, results from comparative immunology have called into question the evolutionary benefits of vertebrate adaptive immunity as a defence mechanism, raising the possibility of alternative evolutionary explanations. For instance, the hypothesis that managing the complex and often beneficial host-microbiota associations characteristic of the vertebrate gut may have favoured the evolution of adaptive immunity. Here, we use individual-based simulations to investigate co-evolutionary interactions between hosts and their microbiota and the implication for the evolution of adaptive immunity. We focus on the capacity of adaptive immunity to produce and modify a diverse repertoire of immune receptors by using somatic variation and selective clonal reinforcement, in combination with a reinforcement bias from the innate immune system. Strikingly, we find that a high diversity of rapidly evolving parasites is insufficient to favour the evolution of adaptive immunity. Instead, our findings suggest that neutral and beneficial microbes can play a crucial role in weakening selection on innate immune defence against parasites in favour of the exploitation of beneficial microbes. In turn, this facilitates the emergence of adaptive immunity as a mechanism reducing the risk associated with infrequent parasite infections while exploiting beneficial microbes. In addition, we show that adaptive immunity can subsequently alter selection affecting both innate immune defence and microbe evolution, such that its loss becomes increasingly unlikely with evolutionary time. Together, these results suggest that simultaneous interactions with diverse mutualists and parasites is a compelling selective explanation for the emergence and maintenance of adaptive immunity.