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Worker bees turn selfish to pass on dad’s genes

A study of worker honey bees suggests the genes they inherit from their queen—matrigenes—direct worker bees’ altruistic behavior. But when the queen dies, the genes they inherit from their fathers—patrigenes—direct them to selfishly compete with one another to lay eggs.

The findings provide strong support for the long-standing, but hotly debated, evolutionary theory of kin selection, which suggests that altruistic behavior occurs as a way to pass genes to the next generation.

“We usually think of honey bees as ideal cooperators, with all the members of the colony working together harmoniously,” says Christina Grozinger, professor of entomology at Penn State. “Our studies demonstrate that there is actually conflict—called intragenomic conflict—among the genes inherited from the father and those inherited from the mother.”

According to Grozinger, in a normal colony, the queen lays all the eggs and the workers remain sterile and help raise the queen’s offspring. When the queen dies, the workers either behave altruistically by remaining sterile and helping rear the remaining offspring and the new offspring of their sisters or they behave selfishly by activating their own ovaries and laying their own unfertilized eggs, which develop into males.

“In 2003, David Queller published a key model using kin selection theory that predicted that under queenless conditions in a honey bee colony, the patrigenes would promote selfish behavior in the workers, while the matrigenes would promote altruistic behavior,” says David Galbraith, postdoctoral scholar in entomology.

According to Queller, this conflict is the result of unequal distribution of the matrigenes and patrigenes among the workers.

When the queen dies

All the workers in the colony share the same set of matrigenes. In contrast, because the queen mated with 10 or more males, the workers have different patrigenes. If a worker behaves altruistically and helps rear her sisters’ offspring, she ensures that her matrigenes are passed on.

However, more of her patrigenes pass to the next generation if she behaves selfishly and lays her own eggs.

[Honest pheromones may explain decline in queen bees]

“It is very strange to think that your genes might be fighting with each other based on whether they came from your mother or your father,” says Queller. “Yet, this is just what we found. It turns out that when a queen dies, worker bees behave the way their fathers want them to, producing sons when possible.”

The results appear in the Proceedings of the National Academy of Sciences.

According to Queller, this intragenomic conflict supports the theory of kin selection first proposed by William Hamilton in 1964. Altruism is defined as reducing one’s own reproductive output to help others reproduce. So kin selection theory predicts that altruism will only evolve to help related individuals.

Using kin selection theory, David Haig, a professor at Harvard University, developed models predicting intragenomic conflict, which Queller then extended to social insect societies.

In 2010, however, biologist E.O. Wilson and colleagues published a paper that argued kin selection is not needed for altruistic behavior to evolve.

“While Queller’s model made very specific predictions about the behavior of matrigenes and patrigenes in social insects, it was not possible to test this prediction until modern genomic tools were developed that allowed us to specifically track both matrigenes and patrigenes in the same individual,” says Grozinger.

Honey bee DNA

The researchers created 18 different male-female crosses of two different genetic stocks of honey bees—Africanized bees, which produce larger ovaries, and European bees, which produce smaller ovaries. The crosses enabled the workers to determine which of the genes—those from fathers versus those from mothers—were active in the offspring. The team housed the worker bee offspring without a queen, stimulating some to start producing eggs.

The researchers first demonstrated that worker bees with Africanized fathers and European mothers had larger ovaries and were more likely to become reproductively active than bees with European fathers and Africanized mothers. According to Grozinger, this demonstrated that the reproductive traits of the workers were more strongly influenced by their patrigenes than matrigenes.

“We identified more than 100,000 sections of DNA, called single nucleotide polymorphisms, that were present in the genomes of either the mother or the father, but not both,” says Galbraith. “This exercise enabled us to determine which pieces of RNA in their worker offspring were produced by the matrigenes versus patrigenes.”

[When bees grow up too fast, the colony collapses]

Next, the researchers harvested workers bees’ ovaries and sequenced the entire set of RNA molecules to see which of their inherited genes were expressed to a greater extent.

“We found that expression of the patrigenes, but not matrigenes, was strongly associated with worker egg-laying behavior,” Galbraith says.

According to researchers, they next plan to explore intergenomic conflict in other systems.

“What is amazing about Queller’s model is that it provides very detailed predictions for how matrigenes and patrigenes behave in different social insect species and different contexts—in some cases, matrigenes are the selfish ones,” Grozinger adds.

Scientists from Princeton University, Purdue University, and Washington University in St. Louis collaborated on the study. The National Science Foundation and the John Templeton Foundation provided support.

Source: Penn State