Persistence through resilience: How sexually deceptive orchids make the most of their pollinators.

Abstract

Exploitation of co-operative relationships is found widely in nature and deception can impose acute fitness costs (including death or reproductive loss), so how do these relationships persist? The Australasian Tongue Orchids, Cryptostylis spp. are extreme deceivers: they achieve outstanding pollination rates, eliciting ejaculation from their male wasp pollinator, Lissopimpla excelsa. Here, I use this system to examine individual-level costs and responses to exploitation through field experiments and evaluate population-level responses to sexual deceit using mathematical modelling and a survey of museum and digital records. In my field experiments, I quantify the costs of sperm for orchid pollinators, finding males may become depleted in their lifetime. I also find evidence of localised morphological and behavioural changes in response to orchid deceit. Compared to the same insect species in areas without orchids, male pollinators in areas with orchids have longer antennae, take longer to arrive at an orchid, have shorter orchid mating durations, and have smaller ejaculates. Antennae length does not appear to be a counter-adaptation to deception as it does not confer discriminatory ability. Instead, males with longer antennae had faster response times and were more likely to pollinate orchids. I hypothesise that rather than counter-adaptations, by manipulating population sex-ratios, Cryptostylis orchids enhance the effects of scramble competition in this species: creating males that more readily search for, and pollinate, these orchids. Mathematical modelling shows that a putative 'resilience' trait, haplodiploidy (in which females can reproduce without sperm, albeit only sons), helps exploited pollinators persist when experiencing sperm depletion. Museum and digital records corroborate this finding. I present two models, one from an orchid's and one from a pollinator's perspective. I found that orchids exploiting haplodiploids receive a double advantage: a pollinator resilient to reproductive interference (haplodiploid populations were less likely to become extinct than diploids and had improved female production); and an enhanced supply of males to act as pollinators (orchids that target haplodiploid populations had higher pollination rates than if they were to target diploids). Combined, these findings present a novel mechanism to explain the persistence of costly relationships: resilience. The idea that certain pre-existing life-history traits allow pollinators to cope with exploitation while improving long-term exploiter success.