Abstract
Queens of social insects make all mate-choice decisions on a single day, except in honeybees whose queens can conduct mating flights for several days even when already inseminated by a number of drones. Honeybees therefore appear to have a unique, evolutionarily derived form of sexual conflict: a queen's decision to pursue risky additional mating flights is driven by later-life fitness gains from genetically more diverse worker-offspring but reduces paternity shares of the drones she already mated with. We used artificial insemination, RNA-sequencing and electroretinography to show that seminal fluid induces a decline in queen vision by perturbing the phototransduction pathway within 24-48 hr. Follow up field trials revealed that queens receiving seminal fluid flew two days earlier than sister queens inseminated with saline, and failed more often to return. These findings are consistent with seminal fluid components manipulating queen eyesight to reduce queen promiscuity across mating flights.
Highlights
Seminal fluid is a complex mixture of proteins and metabolites with multiple functions to enhance male reproductive success (Poiani, 2006; Avila et al, 2011)
We identified 1327 (8.6% of the honeybee transcriptome) differentially expressed genes (DEGs) across all pair-wise brain-comparisons between treatment groups in the two subsequent RNA-seq experiments, with an over-representation of up-regulated DEGs in queens exposed to pure seminal fluid or semen (Figure 1—figure supplement 1 and Figure 1—figure supplement 2; see Supplementary file 1 and Supplementary file 2 for the number and identity of DEGs identified in each pair-wise comparison, respectively)
We conducted a series of genetic and phenotypic experiments and found that seminal fluid induces substantial gene expression changes in the brains of honeybee queens and reduces their visual performance within 24–48 hr. Consistent with these effects, a controlled apiary experiment with treatment and control sister queens showed that queens receiving seminal fluid were more likely to get lost during mating flights in spite of embarking on their flights earlier than control queens, as would be expected from queens actively responding to a perceived deterioration of their visual sensitivity
Summary
Seminal fluid is a complex mixture of proteins and metabolites with multiple functions to enhance male reproductive success (Poiani, 2006; Avila et al, 2011). When females mate with multiple males, seminal fluid components can become agents of sexual selection and harm rival ejaculates while others manipulate female physiology to enhance a specific male’s reproductive success (Parker, 1970; Birkhead and Møller, 1998; Chapman et al, 2003a; den Boer et al, 2010). These interactions have been documented in detail in the fruit fly Drosophila melanogaster where seminal fluid promotes fast oviposition and reduces the willingness of females to seek additional copulations (Chen et al, 1988; Liu and Kubli, 2003; Chapman et al, 2003b).
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