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ASU researchers find link between social behavior, maternal traits in bees

One of the puzzling questions in the evolution of bees is how some species developed social behaviors. Arizona State University Life Sciences associate professor Gro Amdam thinks part of the answer can be traced back to bee reproductive traits.

A paper describing Amdam's experiments, "Complex social behavior derived from maternal reproductive traits," is the cover story of the current issue (Jan. 5, 2006) of Nature. Additional authors include M. Kim Fondrk and Robert Page from Arizona State University, and Angela Csondes from the University of California, Davis.

Honeybees live in highly complex communal societies that include divisions of labor among worker bees. Workers are female bees whose jobs include cleaning, maintaining and defending the hive, raising the young and foraging for nectar and pollen.

Other species of bees, like carpenter bees, do not engage in social behavior and instead lead solitary lives. This has prompted researchers to look into how social structures and divisions of labor have arisen in bees from their solitary ancestors. Amdam's research supports the idea that elements of the reproductive behavior of those ancestors evolved to form a basis for social living and divisions of labor.

This insight provides evidence for how complex social behavior evolves--evidence that could have value for studies of social behavior in other animals, possibly even humans.

"How social life emerged from a solitary lifestyle is a fundamental question," Amdam said. "One theory is that social behavior emerged through new evolutionary inventions. Another is that ancestral solitary phenotypes (characteristics of an organism) were the building blocks of social life, providing a foundation from which social forms could be assembled. For bees, our research supports the latter theory."

Amdam's research began as a doctoral dissertation at the Norwegian University of Life Sciences. She continued the work at University of Cali fornia, Davis in 2003 researching the evolution of social behavior and aging in bees.

While at Davis, Amdam met professor Robert Page, who was breeding honeybee strains distinguished by whether the worker bees were more likely to collect pollen or nectar. Besides their differing collecting habits, the strains possessed various other physiological and sense-related traits, but researchers did not understand how these suites of traits emerged.

In 2004, Page came to ASU as director of the School of Life Sciences. Amdam followed him to ASU in 2005. Together, Amdam and Page theorized that foraging behavior could have something to do with reproductive differences in the worker bees of the two strains.

"Worker bees--which are exclusively female--are considered to be 'facultatively sterile,' meaning that when a queen is present, they do not lay eggs," Amdam said. "However, if the queen is removed, some of these females develop their ovaries and lay eggs."

Foraging for pollen is a maternal reproductive behavior in solitary species of bees, while non-reproductive solitary bees feed mostly on nectar. Amdam wondered if similar relationships were present in the highly social worker bees. She noticed that a certain protein--called vitellogenin--associated with a bee's reproductive status was more common in the strain of bees that preferred to forage for pollen (identified by Amdam as the high pollen-hoarding strain). Low levels of this protein were associated with bees that foraged mostly for nectar (the low pollen-hoarding strain).

Using that as a foundation, Amdam and Page hypothesized that that the high pollen-hoarding strain of social worker bees, although non-reproductive, represented the maternal, reproductive state of its solitary ancestors, who presumably foraged for pollen when reproductively active. By contrast, the low pollen-hoarding strain of worker bees represented the state of those same ancestors when they were not reproduc tively active.

Due to the emergence of colonies with queens responsible for reproduction, the ancestral foraging states were no longer linked to reproductive activity in worker bees, predicted Amdam. But the states could still influence foraging behavior, resulting in a division of labor between pollen-foraging and nectar-foraging worker bees.

To test this hypothesis, Amdam set up a race of sorts to determine which strain of worker bees became reproductively active the fastest. She separated the high and low pollen-hoarding strains into "teams," with the high pollen-hoarding strain representing the ancestral maternal reproductive state, and the low pollen-hoarding strain representing the non-reproductive state. If her hypothesis were correct, the high pollen-hoarders would win the race and develop ovaries sooner than the low pollen-hoarders.

Amdam's prediction proved to be correct when after 10 to 21 days, 76 percent of the high pollen-hoarding strain had developed active ovaries, compared to 42 percent of worker bees in the low pollen-hoarding strain. Students working with Amdam also noticed that the winning strain of worker bees was characterized by larger ovaries, which would contribute to greater reproductive output, furthering the case that foraging behavior was tied to reproductive traits.

Amdam then put her results to a crucial test -- wild-type bees (bees that had not been used in the experiment) were captured after their first foraging flight. Amdam and her team recorded what the bees brought back from the forage and measured their ovaries.

Results from the experiment validated her hypothesis, showing that pollen collection was primarily conducted by worker bees with larger ovaries, cementing the connection between high pollen-hoarding strains and reproductive traits. Amdam also found it remarkable that other physiological traits known to differ between the two strains also correlated with ovary size in the experimen t.

The success of Amdam's research could prove more far-reaching than just the evolution of bee social behavior--scientists can use the findings as a stepping stone when looking at the social evolution of other animals.

"Our findings identify a bridgehead between solitary and social behavior," Amdam said. "If we can understand the emergence social behavior in one system, we can use this insight to create a more general model. Once we have a general model, we can build new hypotheses that outline how similar principles might apply to other animals."


Source:Arizona State University

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