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The Surprising Benefit of Laying Workers

- October 1, 2018 - Alison McAfee

honey bee cells

Laying workers are usually unwelcome pests, but they are also a window into how insect societies may have evolved.

I didn’t understand why my queen cell builder wasn’t rearing any of my grafts. I usually have a deft grafting hand and expected the bees to start drawing out around 90% of yesterday’s queen cups into elegant fingers when I checked on them, but instead they were all cleaned out. Every single one of them. Spick and span.

I started to check the other frames in the builder. Could there be a rogue queen that I accidentally shook in? Or not enough food in the colony? Peering into the comb, I saw something unusual – about 7 or 8 eggs all piled on top of each other in a single cell. If that wasn’t enough of a clue, a few cells over, my eyes locked on to a worker casually shoving her backside into a cell, popping an undignified squat in broad daylight. That worker was laying eggs.

Laying workers are a nuisance to get rid of. It’s usually impossible to spot them, unless you’re lucky enough to catch them in the act of laying. If they’re around, the colony can dwindle into dysfunction. In that sense, they are a lot like social parasites – taking advantage of the colony’s resources to further their own reproduction, while the colony itself fails. Colonies with unusually high occurrences of laying workers have been reported in the US, the UK, New Zealand, Australia, and China. Most people despise these social parasites. But others want to understand them.

Last August, I had the pleasure of joining about a thousand other social insect scientists at the International Union for the Study of Social Insects (IUSSI) quadrennial conference held in Guarujá, Brazil.1 Ben Oldroyd, a professor at the University of Sydney, Australia, was the opening plenary speaker. He has devoted his career to understanding the mechanisms behind social cohesion in honey bees, that is, how and why honey bee workers evolved to be altruistic, or perform behaviors that benefit another individual at one’s own expense. Unlike laying workers, which are very rare in most honey bee colonies, normal, sterile workers selflessly give up their own ability to reproduce in favour of caring for their queen and nestmates.

But this sacrifice of reproductive potential isn’t actually “selfless” at all. Charles Darwin pondered the topic of worker sterility in the social insects as early as the mid-1800s, but an explanation for the evolution of worker sterility wasn’t provided until the 1960s by William Hamilton. Hamilton argued that a decrease in an individual’s fitness can still be evolutionarily favourable provided that it increases the fitness of kin. To illustrate the point, John Haldane, who worked out some of the early mathematics behind this claim, joked that he “would willingly die for two brothers or eight cousins.” In other words, the individual’s direct fitness decreases, but the indirect fitness (the ability of genetic relatives to survive and reproduce) increases, making the trade-off evolutionarily favourable. Soon, this concept of “inclusive fitness” became known as “kin selection.” In this light, a sterile worker honey bee’s dedicated care of her siblings, who either go on to reproduce (queens and drones) or continue the cycle of sibling care (workers) is not selfless, but a worthwhile sacrifice.

This sacrifice makes sense in the context of insect societies, where every individual in the colony is highly related to one another. But in the beginning, how did worker sterility evolve? It is a pivotal biological change that had to occur to enable complex colony life, and its multiple origins in the tree of life has puzzled evolutionary biologists for decades. Understanding it would be a major step in untangling how these societies came to exist millions of years ago. “It’s a long-standing evolutionary question,” says Isobel Ronai, who recently completed her PhD in Oldroyd’s lab. Kin selection theory explains why worker sterility evolved, but how did worker sterility evolve? What genetic changes could have enabled this? Isobel devoted her degree to answering these questions.

Many years ago, Oldroyd bred a line of “Anarchistic” honey bees by artificially inseminating queens with semen from related worker-laid drones. Doing this over and over resulted in a line of honey bees that had a large number of laying workers and all their accompanying dysfunction, making it easier to find out the genetic basis of worker sterility. “The colonies were just incompetent,” Oldroyd told the audience. This line of bees was exactly what the researchers needed.

By comparing these Anarchistic workers to normal, sterile workers, Oldroyd and his team could begin to pinpoint the genetic basis of worker sterility, and therefore eusociality: the holy grail for anyone studying social evolution. Any genetic difference between the Anarchistic and normal workers was a clue about which genes might have been important for enabling insect societies to evolve. “Thousands of [research] papers mention ‘genes for altruism’,” Oldroyd says, “but nobody knew what they were.”

Using this Anarchistic line, Oldroyd’s group found several candidate ‘genes for altruism’ that could be involved in worker reproduction. When Ronai and her colleagues investigated these genes in reproductive and non-reproductive workers, she found that expression of just one of these genes was able to predict whether the worker’s ovaries had eggs, with almost 90% accuracy. This is remarkably high predictive power for genetics. Naturally, they named this gene “Anarchy.” In their paper describing these results, published in the journal Molecular Biology and Evolution,2 they showed that non-reproductive workers produce high levels of Anarchy, while reproductive workers produce very little (because of a confusing quirk of genetics nomenclature, genes are sometimes named after what happens when they are not expressed). Next, they wanted to know how it worked.

One way to gain clues about a gene’s function is to look at exactly where it is expressed. Is it in the brain? The gut? Is it in the ovary? To answer this question, Ronai and her colleagues ….