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It All Began at UC Davis
The highly acclaimed research published in Current Biology that cracked the 200-year secret of complementary sex determination in honey bees is rooted right here, right here at UC Davis.
Arizona State University Provost Robert E. Page, Jr., emeritus professor and former chair of the UC Davis Department of Entomology, and two other UC Davis-affiliated scientists are among the key members of the scientific team from the United States, Germany and France who published their work, “Gradual Molecular Evolution of a Sex Determination Switch in Honeybees through Incomplete Penetrance of Femaleness" in the prestigious journal.
The ground-breaking research shows that five amino acid differences separate males from females.
Lead author is Martin Beye, who was a Fyodor Lynen Fellow in Page's UC Davis lab from 1999 to 2000. He's now an evolutionary geneticist at the University of Duesseldorf, Germany. Another co-author is Michael "Kim" Fondrk, bee breeder-geneticist, who tends Page's research bees at the Harry H. Laidlaw Jr. Honey Bee Research Facility, UC Davis. Fondrk provided the genetic material from crosses from Page's bees.
Page traces the bee puzzle "back to Johann Dzierson in the mid-1800s through Mendel, through Harry Laidlaw to me and to my former postdoc at Davis, Martin Beye."
“Much of the work was done at UC Davis beginning in 1990,” said Page. While at UC Davis, "Martin began the sequencing and characterization of the csd gene; the paper was eventually published as a cover article in Cell."
Said Fondrk: “This project was a long time in making; it began soon after our Cell paper was published in 2003. First we needed to assemble variation for alleles at the sex locus, by collecting drones from many different, presumably unrelated queens, and mating one drone each through an independently reared set of queens using instrumental insemination (which was Fondrk's task). "Then a second set of crosses was made to identify and isolate individual sex alleles. The progeny that resulted from this cross were taken to Germany where Martin Beye’s team began the monumental task of sequencing the sex determination region in the collected samples.”
Silesian monk Johann Dzierson began studying the first genetic mechanism for sex determination in the mid-1800s. Dzierson knew that royal jelly determines whether the females will be queen bees or honey bee colonies, but he wondered about the males.
Dzierson believed that the males or drones were haploid--possessing one set of chromosomes, a belief confirmed in the 1900s with the advent of the microscope. In other words, the males, unlike the females, came from unfertilized eggs.
“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,” Coulombe pointed out.
Coulombe quoted Page: “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. 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 18-20 alleles and find out what regions of these genes are responsible among these variants.”
“What the authors found,” wrote Coulombe, “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.”
Page explained: “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.”
In addition to Beye, Page and Fondrk, other co-authors are Christine Seelmann and Tanja Gempe of the University of Duesseldorf; Martin Hasslemann, Institute of Genetics at the University of Cologne, Germany; and Xavier Bekmans with Université Lille, France
Page, recognized as one of the world’s foremost honey bee geneticists, is a highly cited entomologist who has authored more than 230 research papers and articles centered on Africanized bees, genetics and evolution of social organization, sex determination and division of labor in insect societies. His work on the self-organizing regulatory networks of honey bees is featured in his new book, The Spirit of the Hive: The Mechanisms of Social Evolution, published in June 2013 by Harvard University Press.
Page received his doctorate in entomology from UC Davis in 1980. He left his faculty position at Ohio State University in 1989 to join the UC Davis Department of Entomology faculty. Page chaired the UC Davis department from 1999 to 2004 when ASU recruited him as the founding director and dean of the School of Life Sciences, an academic unit within College of Liberal Arts and Science (CLAS). Page was selected the university provost in December. He had earlier served as the vice provost.
The news story is gathering lots of interest, and rightfully so. It's a piece of a puzzle that went missing for 200 years.
Said Extension apiculturist Eric Mussen of the UC Davis Department of Entomology and Nematology, who was not involved in the research but knows many of the scientists and their work: "Once again, the studies by Dr. Rob Page and his colleagues have unraveled another mystery of honey bee development. It would be interesting if someone investigated the same type of sexual dimorphism in other hymenopterans to determine if they all use the same, ancient-based mechanism.”
Bee breeder-geneticist Michael "Kim" Fondrk works the Page bees in a Dixon almond orchard. (Photo by Kathy Keatley Garvey)
The Spirit of the Hive
That's the title of a newly published book written by Robert E. Page Jr., one of the world's foremost honey bee geneticists.
In his 224-page book, published by Harvard University Press, Page sheds light on how 40,000 bees, "working in the dark, seemingly by instinct alone, could organize themselves to contstruct something as perfect a a honey comb."
Page, former professor and chair of the UC Davis Department of Entomology, marvels at how bees can accomplish these incredible tasks. In synthesizing the findings of decades of experiments, he presents "a comprehensive picture of the genetic and physiological mechanisms underlying the division of labor in honey bee colonies and explains how bees' complex social behavior has evolved over millions of years," according to the Harvard University flier.
Page, now vice provost and dean of the Arizona State University's College of Liberal Arts and Sciences and Foundation Professor of Life Sciences, still keeps his specialized stock of honey bees at the Harry H. Laidlaw Jr. Honey Bee Research Facility at UC Davis. Bee breeder-geneticist Michael “Kim” Fondrk, who worked with Page at Ohio State University, UC Davis and ASU, manages the stock.
In his book, Page talks about the coordinated activity of the bees and how worker bees respond to stimuli in their environment. The actions they take in turn alter the environment, Page says, and "so change the stimuli for their nestmates. For example, a bee detecting ample stores of pollen in the hive is inhibited from foraging for more, whereas detecting the presence of hungry young larvae will stimulate pollen gathering."
Division of labor, Page says, is an inevitable product of group living because "individual bees vary genetically and physiologically in their sensitivities to stimuli and have different probabilities of encountering and responding to them."
Page, who received his doctorate in entomology at UC Davis in 1980, served as an assistant professor at Ohio State University before joining the UC Davis Department of Entomology in 1989. He chaired the department for five years, from 1999 to 2004.
In 2004--the year Page retired from UC Davis--ASU recruited him as the founding director and dean of the School of Life Sciences. At the time, his duties included organizing three departments—biology, microbiology and botany, totaling more than 600 faculty, graduate students, postdoctoral fellows and staff--into one unified school.
As its founding director, Page established the school as a platform for discovery in the biomedical, genomic and evolutionary and environmental sciences. He also established ASU’s Honey Bee Research Facility.
Page is a highly cited author on such topics as Africanized bees, genetics and evolution of social organization, sex determination, and division of labor in insect societies.
Add this one to the list: The Spirit of the Hive.
The queen and her court. (Photo by Kathy Keatley Garvey)
Queen cells. (Photo by Kathy Keatley Garvey)
Turning a Page in Entomological History
The ESA Governing Board today announced the new fellows, who will be recognized Nov. 11, 2012 at the ESA’s annual meeting in Knoxville, Tenn.
Page, the vice provost and dean of the College of Liberal Arts and Sciences, Arizona State University, Tempe, since July 2011, is a pioneer in the field of evolutionary genetics and the social behavior of honey bees.
Page did much of his research at UC Davis. He received his doctorate in entomology at UC Davis in 1980, learning from his major professor Harry H. Laidlaw Jr. (for whom the UC Davis bee research facility is named). He then joined The Ohio State University faculty before returning to UC Davis as a faculty member in 1989.
He chaired the UC Davis Department of Entomology from 1999 to 2004.
Page, who studies the evolution of complex social behavior in honey bees, from genes to societies, left UC Davis in 2004 to be the founding director of the new School of Life Sciences. Arizona State University, where he built a Social Insect Research Group that is now recognized worldwide.
Page was trained as an entomologist, evolutionary population geneticist, classical animal breeder, and mechanistic behaviorist, according to a news release issued by the ESA. "This training has defined his research approach of looking at the genetics and evolution of complex social behavior. He has taken a vertical approach to understanding the mechanisms of honey bee social foraging and how it evolves."
His work is contained in more than 225 research articles. Page has also co-edited three books and authored or co-authored two. Page is a highly cited ISI (Institute for Scientific Information) author in plant and animal science. He is a fellow of the American Association for the Advancement of Science (AAAS) and an elected member of the American Academy of Arts and Sciences, the German National Academy of Science, and the Brazilian Academy of Science. In 1995 he was awarded the Alexander von Humboldt Research Prize by the government of Germany.
Although Page resides in Arizona, his research bees are UC Davis-based residents. Bee breeder-geneticist Michael “Kim” Fondrk, who worked with Page at Ohio State University, UC Davis and ASU, manages the specialized genetic stock, which today includes 90 hives.
Of the 90 hives, about 70 have instrumentally inseminated queens as part of their pollen-hoarding breeding research program.
Back in 2006, Page told us: "Davis is still home to me. I raised my family there, my closest friends and colleagues are still in the entomology department there. I still feel very strong attachments.”
Former department chair Robert Washino remembers him fondly. He recently recalled that "Rob chose to return to UC Davis in 1989 to be with his former major professor (Harry H. Laidlaw Jr.). He later cared for him and his wife, Ruth, in their declining years. We all remember Rob’s scholarly side and his humanitarian side.”
Page joins three other UC-affiliated entomologists in the ESA Fellows Class of 2012: Joseph Morse, professor of entomology at UC Riverside; Henry H. Hagedorn, who received his doctorate in entomology from UC Davis in 1970; and R. Michael Roe, who trained at the UC Davis Department of Entomology from 1981 to 1984 as a National Institutes of Health fellow in cellular and molecular biology.
And interestingly enough, Page is following in the footsteps of Harry H. Laidlaw Jr., who himself was elected an ESA fellow in 1991.
With the addition of Page, the UC Davis Department of Entomology now has 16 fellows who are current or former faculty members. The first was Richard M. Bohart (1913-2007), for whom the Bohart Museum of Entomology is named. He received the honor in 1947. Fifteen others followed: Donald McLean, elected in 1990; Harry H. Laidlaw Jr. (1907-2003), 1991; John Edman, 1994; Robert Washino, 1996; Bruce Eldridge, 2001; William Reisen, 2003; Harry Kaya, 2007; Michael Parrella and Frank Zalom, 2008; Walter Leal, 2009; Bruce Hammock and Thomas Scott, 2010; James R. Carey and Diane Ullman, 2011, and now Robert E. Page Jr., 2012.
Bee breeder-geneticist Kim Fondrk of UC Davis manages the Robert Page specialized genetic stock. These bee hives were in a Dixon almond orchard. (Photo by Kathy Keatley Garvey)
Springing Into Action at the Laidlaw Facility
It's not spring, but don't tell that to the folks at the Harry H. Laidlaw Jr. Honey Bee Research Facility at the University of California, Davis.
Today bee breeder-geneticist Michael "Kim" Fondrk mowed the lush green grass around the apiary. Bee breeder-geneticist Susan Cobey, manager of the Laidlaw facility, continued preparing for a series of specialized bee courses. She tended the hives with beekeeper and junior specialist Elizabeth Frost and beekeeper Tylan Selby, a first-year entomology student.
The conference room buzzed with ideas for an upcoming tour. Following the meeting, Extension Apiculturist Eric Mussen of the UC Davis Department of Entomology faculty talked "bees 'n almonds" with Tabatha Yang, education and outreach coordinator for the Bohart Museum of Entomology on the UC Davis campus. Yang will be conducting the first of what will probably be many tours at the Laidlaw facility.
The tours will include the half-acre Häagen-Dazs Honey Bee Haven and the quarter-acre Campus Buzzway. Both are bee friendly gardens that will provide a year-around food source for the bees, and educational opportunities for visitors.
Meanwhile, oblivious to the people activity, the bees continued to gather pollen and nectar from nearby almond trees.
"The queen bees are really busy laying eggs," Cobey said. That means more workers, more drones and more queen bees.
During the peak season, a queen bee can lay 2000 eggs a day, Cobey said.
That's definitely springing into action.
Kim Fondrk
Examining Almond Blossoms
Lovely almond blossoms
Italian Bee
White Gold
Almond pollination season is approaching, and with it, come concerns.
"A concern each year...is how many honey bee visitation hours occurred during bloom," writes Extension Apiculturist Eric Mussen in his newly published edition of from the UC Apiaries.
Mussen, a former New Englander who has seen dozens of almond pollination seasons in California (he's been a member of the UC Davis Department of Entomology since 1976), says California now has approximately 710,000 acres of almonds. Each acre requires two hives for pollination.
Since California doesn't have that many bees, beekeepers from around the country truck in their colonies. The going rate per hive over the last several years has ranged from $100 to $150.
Generally, California's almond pollination season starts around Feb. 10, Mussen says, and ends around March 10. That takes into account the early, mid- or late varieties that bloom at different times. However, the pollination period for each individual orchard is around 10 days.
The flight hours of a honey bee during almond pollination season? Approximately nine hours a day over a 10-day bloom period.
And what are flight hours? Mussen defines "flight hours" as "the number of hours above 55 degrees when the wind is less than 15 miles per hour, given a sufficient level of sunlight without rainfall."
"I believe that if the tree varieties overlap well in bloom, the bees usually have moved the pollen around in the morning and early afternoon on good flight days," he writes in his newsletter. "That probably requires only about four hours a day."
Of course, poor weather can interfere significantly with "fertilization and nut set," Mussen says, "but it would not be the fault of the bees."
As a service to beekeepers and growers, a retired beekeeper posts information on the Almond Board of California Web site indicating who's renting colonies and who needs pollination.
Meanwhile, check out the images below of UC Davis bee breeder-geneticist Kim Fondrk in a Dixon, Calif. almond orchard. Fondrk manages the Honey Bee Pollen Hoarding Selection Program at the Harry H. Laidlaw Jr. Honey Bee Research Facility, UC Davis, under the direction of Robert E. Page Jr., Arizona State University. Fondrk and Page moved the bees from Arizona to California several years ago.
Almond Orchard
Kim Fondrk
Honey Bee
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