ASU research answers 200-year-old question of sex determination in bees

December 30, 2013

It’s taken nearly 200 years, but collaborators in Arizona and Europe have teased out how the molecular switch for sex gradually and adaptively evolved in the honeybee. 

The first genetic mechanism for sex determination was proposed in the mid-1800s by a Silesian monk named Johann Dzierson, according to the study’s co-author and Arizona State University Provost Robert E. Page Jr. ASU Provost Robert E. Page Jr worked with honey bees, scientists in Europe Download Full Image

Dzierson was trying to understand how males and females were produced in honeybee colonies. He knew that the difference between queen and worker bees – both females – emerged from the different quality and quantity of food. But, what about the males, he asked.

Dzierson posited that males were haploid – possessing one set of chromosomes, which was confirmed in the 1900s with the advent of the microscope. Under the magnifying lens, researchers could see that eggs that gave rise to drones were not penetrated by sperm. However, how this system of haplodiploid sex determination ultimately evolved at a molecular level has remained one of the most important questions in developmental genetics.

In the December issue of Current Biology, Page and Martin Beye, lead author and professor with the Institute of Evolutionary Genetics in the University of Duesseldorf, Germany, and their collaborators laid out the final pieces of how these systems evolved in their article, “Gradual molecular evolution of a sex determination switch in honeybees through incomplete penetrance of femaleness.”

The authors studied 14 natural sequence variants of the complementary sex determining switch (csd gene), for 76 genotypes of honeybees. 

While complex, the researchers had several tools at hand that their predecessors lacked to solve this sexual determination puzzle. First, honeybees are ideal study subjects because they have one gene locus responsible for sex determination. Also, Page and former graduate student Greg Hunt identified genetic markers – well-characterized regions of DNA – close to the complementary sex determining locus to allow gene mapping.

In addition, Hunt and Page found that the honeybees’ high recombination rate – the process by which genetic material is physically mixed during sexual reproduction – is the highest of any known animal studied, which helped Beye isolate, sequence and characterize the complementary sex determining locus.

Page and Beye also were able to knock out an allele and show how one could get a male from a diploid genotype – work that was featured on the cover of the journal Cell in 2003. 

However, the questions of which alleles were key, how they worked together and in what combinations, and why this system evolved were left unanswered, though tantalizingly close. This compelled the current team of collaborators to step back to review what actually constitutes an allele. 

“There has to be some segment of that gene that is responsible in this allelic series, where if you have two different coding sequences in that part of the gene you end up producing a female,” said Page. “So we asked how different do two alleles have to be? Can you be off one or two base pairs or does it always have to be the same set of sequences? We came up with a strategy to go in and look at these 18 to 20 alleles and find out what regions of these genes are responsible among these variants.”

“In this process, we also had to determine if there are intermediate kinds of alleles and discover how they might have evolved,” added Page.

What the authors found was that at least five amino acid differences can control allelic differences to create femaleness through the complementary sex determiner (csd) gene – the control switch. 

“We discovered that different amounts of arginine, serine and proline affect protein binding sites on the csd gene, which, in turn, lead to different conformational states, which then lead to functional changes in the bees – the switch that determines the shift from female to not female,” said Page.

The authors also discovered a natural evolutionary intermediate that showed only three amino acid differences spanned the balance between lethality and induced femaleness. These findings, which have taken nearly 200 years of study to pin down, suggested that incomplete penetrance may be the mechanism by which new molecular switches can gradually and adaptively evolve.  

In addition to Beye and Page, authors included Christine Seelmann and Tanja Gempe with the University of Duesseldorf, Martin Hasslemann with the Institute of Genetics at the University of Cologne in Germany, Xavier Bekmans with Université Lille in France and Kim Fondrk with Arizona State University. The work was supported by grants from the Deutsche Forschungsgemeinschaft.

Page is the Foundation Chair of Life Sciences at ASU, a professor in the School of Life Sciences and the author of "The Spirit of the Hive: The mechanism of social evolution," published by Harvard University Press in 2013. 

Margaret Coulombe

Director, Executive Communications, Office of the University Provost


ASU student wins Fulbright-Hays Scholarship to China

December 30, 2013

Maria Chappell, an ASU senior majoring in anthropology and Chinese, has been awarded a Fulbright-Hays Scholarship to study in China to improve her Chinese language and cultural knowledge.

Chappell, a Glendale native, will spend the spring semester working on research projects at Shaanxi Normal University in Xi’an – one of the oldest cities in China – located in the Shaanxi province, where along with studying Chinese language and culture, she will take classes in Chinese boxing and a two-stringed bowed musical instrument called Erhu. The visit will include a six-week internship during the summer at Xi’an High Technology Development Zone. The Cortez High School graduate will also celebrate the Chinese New Year with a Chinese family and plans on visiting Yunnan and Shangri-La to experience Tibetan culture. Download Full Image

“With the help of the Fulbright-Hays scholarship, I will be able to immerse myself in Chinese language and culture, and become an observer of life in China,” said Chappell. “The opportunity will allow me to form connections and, eventually, relationships with the natives and absorb the insight they have to offer.”

But learning about Chinese language and culture wasn’t the first choice for Chappell. She had initially hoped to focus her attention on archaeology and ancient Mesoamerica.

“However, I decided that I was more interested in a cultural anthropological look at China, since it is one of the most pivotal, modern-day cultures in the world,” she said. “I subsequently enrolled in the Chinese Language Flagship Program at the School of International Letters and Cultures and haven’t looked back." The School of International Letters and Cultures is within the College of Liberal Arts and Sciences.

For Chappell, understanding culture and how it affects a person’s life direction and reaction to various circumstances is fascinating.

“Studying anthropology and Chinese language has made me realize that there is more to the world than just the American way of looking at things,” she said. “But, along with the differences, you also start to notice the similarities in cultures and realize that we are not that different after all.”

Business anthropology is another related subject that interests the bright and promising ASU senior, who plays double-reed musical instruments as a hobby. She wants to become a cross-cultural business consultant after graduation.

“If a company in the U.S. wishes to start a business in China, in order to be successful, it would have to be familiar with marketing tactics and business practices that align with Chinese culture and values. That is where business anthropology comes in handy.”

Understanding cultures and decision-making processes and motivations makes Chappell tick, and she is happy to have pursued her topics of interest at ASU.

“The ASU community has provided me opportunities to pursue my dreams,” she said. “I hope to never stop moving forward. I want to keep getting better and learn more.”

The Fulbright-Hays Scholarship is funded by the U.S. Department of Education Fulbright-Hays GPA Program and granted through Associated Colleges in China (ACC), a partnership of six leading institutions of higher education in China. It is awarded to deserving U.S. undergraduate or graduate students to sponsor tuition, travel and living expenses in China.

Media projects manager, Office of Knowledge Enterprise Development