Controlling Bee Fate
Reversible marks on the genome allow honeybees to 
swap between lives as nurses and foragers.
By Ed Yong
The Scientist
September 16, 2012
http://the-scientist.com/2012/09/16/controlling-bee-fate/

Honeybee workers can flip back and forth between two
careers, thanks to a small number of reversible
epigenetic changes. Researchers from the Johns Hopkins
School of Medicine and Arizona State University showed
that the switch from young nurse bees, which stay in the
hive to care for grubs, to older travelling foragers
involves a set of epigenetic marks that affect how a
small number of genes are used. And if the foragers
change back into nurses, the marks revert, too.

The results, published today (September 16) in Nature
Neuroscience, are the first to show that two patterns of
behavior are associated with reversible epigenetic
changes.

"Behavioral biologists talk readily about adaptive
plastic behaviors that allow an organism to respond to
its immediate environment," said Seirian Sumner, a
behavioral ecologist at the Institute of Zoology,
London, who was not involved in the study. "This paper
is the first step in exposing the mechanisms, and making
them possible to study."

"This is one of those papers that makes me envious,"
said David Sweatt, a neurobiologist from the University
of Alabama at Birmingham, who was not involved in the
study. "I feel it will be a foundational paper in the
nascent field of behavioral epigenetics."

Brian Herb, a student in Andrew Feinberg's lab at the
Johns Hopkins School of Medicine, started by comparing
one type of epigenetic change-DNA methylation-in the
brains of five queens and five workers. Even though
another research group had published 550 genes with
methylation differences between these two castes, Herb
found none.

"We thought that we were asking the wrong question since
a queen never turns into a worker," said Feinberg.
"That's not flexible." Within the worker caste, however,
are nurse bees and foragers. "Bees start off as nurses
and then become foragers," said Gro Amdam of Arizona
State University, who co-authored the study. "It's as
different as being a scientist or journalist. It's
really amazing that they can sculpt themselves into
these two roles that require very specialist skills."

When Herb compared the methylation patterns of nurses
and foragers, he found differences in 155 genes. These
were largely involved in controlling the activity of
other genes, packaging DNA into chromatin or cutting up
RNA transcripts. "They look like genes that are
regulating plasticity," said Feinberg.

Next, Florian Wolschin, a postdoc in Amdam's lab,
removed all the nurses from the team's hives while the
foragers were away. "The foragers come back and go, `Oh
no, what happened?' Half of them turn back into nurses,"
said Feinberg. "Their bodies change a little bit and
their behavior's completely different." Such reversals
are rare in the wild, but they can happen when hives
split up and old queens leave with young workers to
found new colonies. The new queens inherit existing
nests that are devoid of young nurses, and some old
foragers revert roles to fill the employment gap.

The team found that methylation patterns in 107 genes
changed during the forager-to-nurse reversion, 57 of
which overlapped with the nurse-to-forager set. Although
Sumner points out that the sample size is "scraping the
statistical barrel," the team did repeat their
experiment with a fresh set of bees and found the
methylation in 45 of the same 57 genes changed with both
role switches.

About half of the methylation changes seem to silence
the genes they mark, and others change the way the RNA
transcripts of other genes are spliced. "A nice
mechanistic flow chart is emerging," said Sumner.
Environmental triggers lead to changes in methylation
that influence how genes are expressed or processed,
leading to changes in behavior. "This pretty much
describes a behavioral genomicist's dream!" she added.

Sumner points out that the shift from nursing to
foraging can happen over a matter of hours- a seemingly
easy change despite the stark differences in behavior.
She now wants to know if animals that show stronger
shifts in behavior throughout their lives would have
more dramatic epigenetic changes too. "At what point
does behavioral reversibility become an irreversible
unidirectional shift?" she wondered.

B. R. Herb et al., "Reversible switching between
epigenetic states in honeybee behavioral subcastes,"
Nature Neuroscience, doi:10.1038/nn.3218, 2012.

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