Orchid sexual deceit affects pollinator sperm transfer

Abstract

Abstract For many animals, sperm can be a limiting resource and impact lifetime reproductive success. Sperm limitation can arise from reduced male availability in a population, but may also be a consequence of external influences, such as sperm wastage. If sperm is finite and not always cost‐free to produce, do males vary sperm use strategies in response to sperm limitation? One way to answer this is to examine male sperm allocation in response to sexual deception that elicits sperm wastage. Cryptostylis orchids trick their parasitoid wasp pollinator, male Lissopimpla excelsa, into mating with the flower and ejaculating. For many parasitoids sperm is limited; so this exploitative interaction could impose a high cost to males. Here, we ask whether this duped wasp can become sperm limited, and whether this impacts his ejaculate size following deception. Sperm limitation has implications for his future and lifetime reproductive success, and consequently, the ultimate fitness of the orchid, and the evolutionary maintenance of orchid deception systems in general. We compared sperm use and availability for male L. excelsa wasps from wild populations that either did or did not co‐occur with sexually deceptive Cryptostylis orchids. On average, males had ~50,000 sperm cells in their seminal vesicles and ejaculated ~10% of their existing sperm stock in a single encounter. Pollinators that were permitted to mate with an orchid had significantly less sperm than males that were not, suggesting they may become temporarily sperm limited. Pollinators from sites with orchids ejaculate significantly less sperm on orchids than naïve males. The difference in ejaculate size for pollinators that do and do not co‐occur with orchids may be a consequence of males learning to avoid orchids, or an adaptation to avoid sperm depletion. Alternatively, males may reduce sperm allocation when they perceive more available ‘females’ (either orchids or real females) in the environment. These costs and responses to exploitation show how plants can influence the population dynamics of their pollinators, and, more broadly, provides an explanation for the maintenance antagonistic co‐evolutionary relationships. We suggest that by interfering with the population dynamics of a duped species, exploiters might improve their own persistence. A free plain language summary can be found within the Supporting Information of this article.