The evolutionary ecology of cheating: does superficial oviposition facilitate the evolution of a cheater yucca moth?

Abstract 1. A major question in the study of mutualism is to understand how mutualists may revert to antagonists that exploit the mutualism (i.e. switch to cheating). In the classic pollination mutualism between yuccas and yucca moths, the cheater moth Tegeticula intermedia is sister to the pollinator moth T. cassandra. These moth species have similar ovipositor morphology, but T. intermedia emerges later, oviposits into fruit rather than flowers, and does not pollinate. 2. We tested if the pollinator, T. cassandra, was pre‐adapted to evolve a cheater lineage by comparing its emergence and oviposition behaviour on yucca fruit to a distantly related pollinator, T. yuccasella, that differs in ovipositor morphology and oviposition behaviour. We predicted that if T. cassandra was pre‐adapted to cheat, then these pollinators would emerge later and be able to oviposit into fruit in contrast to T. yuccasella. 3. Contrary to expectations, a common garden‐rearing experiment demonstrated that emergence of T. cassandra was not significantly delayed relative to T. yuccasella. Moth emergence patterns overlapped broadly. 4. No choice oviposition experiments with female moths demonstrated that both pollinator species attempted to oviposit into fruit, but only T. cassandra was successful. Four out of 84 T. cassandra successfully oviposited into older fruit, whereas zero out of 79 T. yuccasella oviposited into older fruit. The rarity of the cheating behaviour in pollinators, however, meant that no significant difference in oviposition ability was detected. 5. The results suggest that a shift in emergence phenology is likely not a pre‐adaptation to the evolution of cheating, but that the ability to successfully lay eggs into fruit may be. The results also demonstrate that cheating attempts are rare in these pollinator species and, hence, the evolutionary transition rate from pollinator to cheater is likely to be low.