Honey bee queens keep sperm from drones alive inside them for years, but some surprising environmental triggers can cause massive sperm death.
“Give the drone’s thorax a pinch,” Jeff Pettis instructed as I took the drone he handed me. “Then squeeze the abdomen between your thumb and forefinger, rolling from the front of the abdomen to the tip.” I flipped the drone upside down and started to pinch the thorax as coached, feeling a crispy crunch as it buckled and killed the bee. I stifled a shudder – I always hate the sensation of crushing an exoskeleton, whether it belongs to a bee or another insect. The drone’s abdomen still pulsed with reflexive breaths, which quickly stopped as I squeezed it from front to back.
Jeff was showing me how to harvest fresh semen from drones. That day, we were just practicing, but semen collected in this way can then be used for instrumental insemination or tested for sperm viability. And sperm viability is a critical determinant of queen quality, and ultimately, colony longevity—dud sperm directly translate into fewer workers, less genetic diversity, and potentially smaller colonies. New research suggests that sperm viability is compromised by common challenges like temperature stress and pesticide exposure, even more than previously thought.
As I squeezed the abdomen, it felt like it was going to explode between my fingers. But sure enough, instead of bursting, the endophallus shot out from the hind end, pausing with two bright orange horns (cornuae) poking out as if someone was blowing into an inside-out rubber glove. It looked truly alien. “That’s a partial eversion,” Jeff confirmed. “Now keep squeezing.”
The rest of the phallus exploded from the abdomen with a pop. Sitting on top of the bulbous end were a few microlitres of creamy café au lait colored semen, poised for collection.
A drone’s purpose in life is to grow big enough and strong enough to compete with other drones for access to a virgin queen during her nuptial flight. If successful, they mate in mid-air, he deposits that drop of semen inside of her (explosive pop included), his phallus rips from his body, and he falls to his death. For every queen, about fifteen to twenty drones mate with her and reach this morbid fate. But while the drones themselves may die, their sperm will live inside the queen for years, fathering millions of offspring over the course of the queen’s life.
How is it possible for sperm to stay alive in the queen for so long, when in other animals, they live only minutes or days? Human sperm, for example, only stays alive outside a male’s body for about twenty minutes (or several days, in the female’s fallopian tube). Queen ants, which are also social insects, put even honey bees to shame; most ant queens store live sperm for upwards of ten years.1
In a social insect’s kingdom, the dogma is not only long live the queen, but also long live the queen’s sperm. Researchers have been searching for the mechanism of these remarkable feats of sperm storage since the 1960s, when Eugenia Alumot, from Rehovot, Israel, began investigating the sugars and enzymes that could be providing honey bee sperm with energy inside the queen’s spermatheca (the specialized organ that stores the sperm).2
Now, we know that after a burst of energy used to out-swim other sperm and gain access to the spermatheca, the sperm fall into a fairly quiescent life. Specific metabolic pathways are dialed back, so once inside the spermatheca, the sperm metabolize nutrients differently. This probably enables them to minimize damage – and cell death – caused by molecules called “reactive oxygen species,” which are by-products of some types of energy-generating metabolism.3 But these carefully tuned metabolic shifts can easily be thrown off-balance.
A few years ago, Jeff Pettis and other researchers found that failing colonies tended to be headed by queens with sub-par sperm viability in their spermathecae. Many of the queens’ precious sperm (almost half of their lives’ supply, in fact) were dead. Pettis and colleagues published a paper in PLoS ONE4 describing how when they dissected spermathecae and looked at the sperm they contained under a microscope, counting how many were alive and dead, the queens heading colonies that were rated as being in “good health” by beekeepers tended to contain sperm with high viability. Around 85-92% of sperm in these queens were still alive. In contrast, queens heading colonies rated as “failing” contained ….