By eliminating the queen, a matricide worker clears the way for worker bees to lay male eggs

One day a few years ago, while working on wasps in a rainforest in Costa Rica, entomologist Kevin J. Loope, a postdoctoral researcher at the University of California, Riverside, began reading about the puzzling matricide behavior of some social insects. In most social insects, such as bees, ants and wasps, the workers, all of which are female, work their entire lives to help the queen produce new offspring. Still, Loope found in the literature anecdotal reports of workers killing their queen, providing a fascinating evolutionary puzzle.

“The observations of queen killing seemed paradoxical to me,” Loope said. “Why does it pay to help the queen in some situations, but also kill her in other situations? What explains why some queens get killed and others don’t, and why kill her at all? Most people think of social insects as workers who thoughtlessly toiling for the good of the queen or the colony, but it seems that workers are more calculating, helping or harming the queen, depending on the circumstances they find themselves in.”

To investigate the puzzle, Loope set up observation colonies of yellow jacket wasps in the lab, filming them continuously using video cameras, and then recording when matricide occurred. He also collected wild colonies to increase the sample size, deriving matricide from mature colonies without queens. The behavioral observations and genetic analyzes of wasp colonies he conducted showed that worker wasps kill queens when in colonies with many full siblings, but not in colonies with a mix of full and half siblings.

“Workers assess the situation in their colony and decide to rebel against the queen only if the genetic makeup of the colony makes it favorable,” Loope said. “The main advantage is that your sister workers can lay male eggs, instead of the queen, who usually stops the worker’s reproduction by eating eggs, attacking reproductive workers and by laying many of her own eggs. By the queen , a matricide worker, allows other workers and herself to lay male eggs.”

Workers do all the tasks of rearing the brood. They search for food, feed the offspring and the queen, build the nest and defend it. Only occasionally do they attempt to reproduce. Males are produced at the end of the year and mate with the new queens. Then the males die. Workers never mate, but can still lay male eggs because of a quirk in their genetic system. This allows them to compete with the queen for the production of males.

“Hence the matricide,” Loope said. “Workers are not mindless automatons working for the queen anyway. They only altruistically give up procreation if the context is right, but revolt if it benefits them.”

The study is one of the few to suggest that workers can assess the relative proportions of their colony’s full and half siblings and respond adaptively when conflicts of interest arise over what the colony should do, for example the sons of workers or the queen’s sons.

“In highly eusocial species, altruism toward the queen is typically unconditional,” Loope said. “However, this study provides the first in-depth investigation of queen behavior, a common but difficult to observe event in the lives of many bee and wasp colonies. I have devised a way to continuously observe colonies using video, which allows for the first video observations of this behavior.”

Study results appear online in Current Biology.

Loope explained that the genetic makeup of a colony is determined by how often a queen mates (usually once or twice), and by how evenly she uses the sperm of two males when she has mated twice. He found that colonies that experienced matricide had a higher proportion of full siblings (as measured by the average relatedness between members of the colony) than those that had not experienced matricide.

“This pattern is determined by the number of times the queens mate, as well as the evenness of sperm use for queens that have mated twice, suggesting that workers can differentiate between these different types of queens,” Loope said. “A queen-killing worker benefits from matricide in lone father colonies because it causes the colony to raise the sons of other workers, rather than the sons of the queen. In such colonies, worker bees are more closely related to worker sons than to queen sons.” .

Kin selection theory, an extension of evolutionary theory, predicts that behavior evolves favoring closer kin over more distant relatives; half siblings are further away than full siblings, so matricide is less beneficial in colonies with many half siblings, Loope added. “Thus, this study provides rare support for kin selection theory with variation in behavior between colonies. Workers respond to their colony composition as predicted by kin selection theory.”

Loope is now trying to understand how the interaction of yellow jacket wasps with other species can shape changes in social organization.

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