Social insects have long been a fascinating puzzle for evolutionary biologists. In these species, the majority of individuals are workers who shut off their ability to reproduce, instead serving the good of the colony. The reason for this selfless sacrifice is usually explained by the relatedness of all the insects in a colony – it can make sense to give up your shot at producing offspring if you have thousands of closely related nieces and nephews. But there's a paradox: reproductive colony queens are extremely promiscuous, a trait that increases colony productivity by increasing genetic diversity, but might also be expected to decrease worker's motivation to suppress their reproduction as it reduces relatedness. So, how is promiscuity in queens selected for? It could occur if workers increased their own reproductive ability in the presence of a monogamous queen, thereby sacrificing the good of the colony by becoming a less productive worker and producing a selection pressure on queens to choose polyandry.
To test this theory, Heather Mattila from Wellesley College, USA, and her colleagues from Cornell University, USA, decided to manipulate the mating of honey bee queens and measure the effects on the reproductive physiology and behaviour of their workers in a report published in Current Biology. They artificially inseminated queens with semen from either a single male bee or a pool generated from 15 bees, ensuring that the total volume of semen was kept constant as workers can detect the volume of semen in a queen's spermatheca. They also allowed some queens to mate naturally (which is always with multiple males). Following mating, they placed all the queens into new colonies.
Two months later, the researchers took a peek at the worker's ovaries by dissecting a sample of workers from each colony. They found that workers who lived in colonies with a queen that had been inseminated with sperm from a single male had ovaries with increased development – a sign that the workers were investing in their own reproductive ability. Meanwhile, workers in colonies where the queen had either received artificial insemination with sperm from multiple males or was naturally mated had a lower probability of having ovaries that had been activated.
As it appeared that workers increased their investment in their own reproduction when their queens had remained monogamous, the researchers decided to investigate what effect this had on how hard the workers worked. They installed a portion of each colony in an observation hive in a greenhouse, where they hung a feeder containing sugar water as a food source. They counted how many trips a day each worker made and how much time each worker spent ‘waggle dancing’ – communicating to the other workers where the food source was located. They found that colonies that had workers with more activated ovaries also had workers that spent far less time visiting the food source and dancing for their colony mates. Furthermore, when the researchers manipulated individual workers to activate their ovaries, they found that these workers were far lazier than untreated workers. So, in short, in colonies where the queen mated with only a single male, the workers increased ovary activation and were far less productive than those in colonies where the queen was inseminated by many males.
While the researchers can't tell from this experiment why workers might be increasing their ovary activation, workers will capitalize on shy queens who don't mate with multiple males by investing in their own reproduction at the cost of colony productivity. So, for the queen, promiscuity is a virtue.