Trade‐off between reproductive and anti‐competitor abilities in an insect–parasitic nematode–bacteria symbiosis

Mutualistic symbionts can provide diverse benefits to their hosts and often supply key trait variation for host adaptation. The bacterial symbionts of entomopathogenic nematodes play a crucial role in successful colonization of and reproduction in the insect host. Additionally, these symbionts can produce a diverse array of antimicrobial compounds to deter within‐host competitors. Natural isolates of the symbiont, Xenorhabdus bovienii, show considerable variation in their ability to target sympatric competitors via bacteriocins, which can inhibit the growth of sensitive Xenorhabdus strains. Both the bacteria and its nematode partner have been shown to benefit from bacteriocin production when within‐host competition with a sensitive competitor occurs. Despite this benefit, several isolates of Xenorhabdus do not inhibit sympatric strains. To understand how this variation in allelopathy could be maintained, we tested the hypothesis that inhibiting isolates face a reproductive cost in the absence of competition. We tested this hypothesis by examining the reproductive success of inhibiting and non‐inhibiting isolates coupled with their natural nematode host in a non‐competitive context. We found that nematodes carrying non‐inhibitors killed the insect host more rapidly and were more likely to successfully reproduce than nematodes carrying inhibitors. Lower reproductive success of inhibiting isolates was repeatable across nematode generations and across insect host species. However, no difference in insect mortality was observed between inhibiting and non‐inhibiting isolates when bacteria were injected into insects without their nematode partners. Our results indicate a trade‐off between the competitive and reproductive roles of symbionts, such that inhibiting isolates, which are better in the face of within‐host competition, pay a reproductive cost in the absence of competition. Furthermore, our results support the hypothesis that symbiont variation within populations can be maintained through context‐dependent fitness benefits conferred to their hosts. As such, our study offers novel insights into the selective forces maintaining variation within a single host–symbiont population and highlights the role of competition in mutualism evolution.