Societies to genes? And how do you get from there to here?
Noted honey bee geneticist Robert E. Page Jr., a UC Davis and Arizona State University emeritus professor and administrator, has authored a newly published, invited article in the journal Geneticson “Societies to Genes: Can We Get There from Here?” that highlights his three-decade scientific career.
“I was thrilled to be invited to write this perspectives/review of my scientific career; it is a collection of 30 years of single-minded focus on one question,” said Page, who is renowned for his research on honey bee behavior and population genetics, particularly the evolution of complex social behavior, and for his work on the first genomic map of the honey bee.
"The editors contacted me to write a perspectives/review that focuses on my own work, a study in complex adaptation,” Page related. “This is the first time they have done a perspectives article like this. I was, of course, honored. More than half of the work was done at UC Davis.”
“Understanding the organization and evolution of social complexity is a major task because it requires building an understanding of mechanisms operating at different levels of biological organization from genes to social interactions,” Page wrote in his abstract. “I discuss here, a unique forward genetic approach spanning more than 30 years beginning with human-assisted colony-level selection for a single social trait, the amount of pollen honey bees (Apis mellifera L.) store. The goal was to understand a complex social trait from the social phenotype to genes responsible for observed trait variation.”
“The approach,” Page wrote, “combined the results of colony-level selection with detailed studies of individual behavior and physiology resulting in a mapped, integrated phenotypic architecture composed of correlative relationships between traits spanning anatomy, physiology, sensory response systems, and individual behavior that affect individual foraging decisions. Colony-level selection reverse engineered the architecture of an integrated phenotype of individuals resulting in changes in the social trait. Quantitative trait locus (QTL) studies combined with an exceptionally high recombination rate (60 kb/cM), and a phenotypic map, provided a genotype–phenotype map of high complexity demonstrating broad QTL pleiotropy, epistasis, and epistatic pleiotropy suggesting that gene pleiotropy or tight linkage of genes within QTL integrated the phenotype. Gene expression and knockdown of identified positional candidates revealed genes affecting foraging behavior and confirmed one pleiotropic gene, a tyramine receptor, as a target for colony-level selection that was under selection in two different tissues in two different life stages. The approach presented here has resulted in a comprehensive understanding of the structure and evolution of honey bee social organization.”
Page, who received his doctorate in entomology (1980) from UC Davis, joined the UC Davis entomology faculty in 1989, and chaired the department from 1999-2004. In 2004, Arizona State University recruited him as founding director of its School of Life Sciences. His career advanced from dean of Life Sciences, to vice provost and dean of the College of Liberal Arts and Sciences, to university provost. Today he holds the titles of ASU provost emeritus, ASU Regents professor emeritus, and UC Davis distinguished emeritus professor, an award bestowed in 2019.
For 24 years, from 1989 to 2015, Page maintained a UC Davis honey bee-breeding program, managed by bee breeder-geneticist Kim Fondrk at the Harry H. Laidlaw Jr. Honey Bee Research Facility. Together they discovered a link between social behavior and maternal traits in bees.
In his article, he mentions: "I studied the behavioral genetics of pollen storage in honey bees for more than 30 years. The effort was collective with my technician and colleague Kim Fondrk and numerous students and postdoctoral researchers. We used a forward genetic approach and employed bidirectional, human-assisted selection that resulted in the establishment of two strains that varied in their expression of a social phenotype. We focused on just one trait, the amount of pollen stored in the nest, a social trait that is a consequence of the interactions of thousands of bees. There are about 10–40 thousand worker bees in a honey bee colony, depending on the time of year. Honey bee colonies have a reproductive division of labor where the single queen normally lays the eggs while the workers are facultatively sterile."
"Young larvae produce pheromones (chemical signals) that stimulate some of the foragers to collect pollen (Traynor et al. 2015)," he explained. "The amount of pollen stored, the number of cells that are full, affects the number of larvae that are raised and inhibits pollen foraging, thus stored pollen is regulated (Fewell and Winston 1992). Returning pollen foragers perform recruitment dances that communicate the distance and direction from the nest to their pollen sources. Other bees attend the dances and are recruited. So, the amount of stored pollen is dependent on the interactions of thousands of individual adults and larvae and is not a phenotypic trait of any individual—it is a social phenotype."
Page has authored than 250 research papers, including five books: among them, The Spirit of the Hive: The Mechanisms of Social Evolution, published by Harvard University Press in 2013. His most recent book is The Art of the Bee: Shaping the Environment from Landscapes to Societies, published by Oxford University Press 2020. (See news release on why bees are both artists and engineers.)
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.
If a queen bee were to celebrate Mother's Day (and she won't because she's too busy laying eggs), what a crowded festivity that would be.
Bee breeder-geneticist Susan Cobey of Washington State University, former manager of the Harry H.Laidlaw Jr. Honey Bee Research Facility at UC Davis, describes the queen as an "egg-laying machine."
"She's the mother of all the bees in the hive," saysCobey, who studied at UC Davis with Harry Hyde Laidlaw Jr., (1907-2003), "the father of honey bee genetics." During the peak season, the queen can lay up to 2000 eggs a day. That amounts to about 50,000 to 80,000 workers (sterile females) and 1000 to 2000 drones (males) in the hive.
On her maiden flight, the queen bee mates with some 12 to 25 drones in mid-air and then she heads back to the hive to lay eggs for the rest of her life, says Cobey, internationally renowned for her Carniolan bees and classes on instrumental insemination and bee breeding (stock improvement).
Yes, every bee in the hive has the same mother. Not so with the fathers.
In his book, The Honey Bee Hobbyist, the Care and Keeping of Bees, Norman "Norm" Gary, UC Davis emeritus professor of apiculture, writes: "All bees in a colony develop from eggs laid by the queen, so they all share the same mother. All bees in a colony develop from eggs laid by the queen, so they all share the same mother. But as a population, they typically have around 15 fathers."
As Gary points out: "The queen bee has no control over the drones that inseminate her. (The virgin queen) mates while flying, never inside the hive."
It's a matriarchal society. The girls (worker bees) do all the work; they serve as nurse maids, nannies, royal attendants, builders, architects, foragers, dancers, honey tenders, pollen packers, propolis or "glue" specialists, air conditioning and heating technicians, guards, and undertakers. So their abbreviated life (during the summer the life span of a worker bee is only four to six weeks) is not surprising. The drones, or males, serve only a reproductive function. Once they they mate, they die.
Honey bee geneticist Robert E. Page Jr., distinguished emeritus professor of entomology at UC Davis (and emeritus provost, Arizona State University) studied with Laidlaw for his doctorate at UC Davis. He pays tribute to Laidlaw in his book, The Art of the Bee: Shaping the Environment from Landscapes to Societies.
In Chapter Nine, "The Song of the Queen," Page reprinted a poem by E. B. White (Dec. 15, The New Yorker) objecting to instrumental insemination. White opined in the poem that the queen bee should "mate with whatever drone" she encounters.
Page reprinted Laidlaw's response, published in the San Francisco Chronicle, which said in part:
Her offspring slave throughout the day,
They feed her children as best they may
They would like to see a moment
Directed toward stock improvement.
If you're interested in bees and beekeeping, or just curious about these amazing superorganisms, these books read well on Mother's Day...and any other day./span>
"I saw the swarm when I looked out the window," said Vacaville resident Lynn Starner. She watched dozens of bees buzzing toward the cluster.
Flowering plum branches sheltered and shadowed the swarm's temporary home, while the intrepid bee scouts searched for a permanent one.
A moving swarm is as fascinating as it is remarkable. "The casual observer sees chaos, but in reality it's organized, moving in circles with scouts flying through the swarm, directing it while it travels at about 11 kilometers per hour," writes renowned honey bee geneticist Robert E. Page Jr. of UC Davis and Arizona State University in his 256-page book The Art of the Bee: Shaping the Environment from Landscapes to Societies.
"They don't go far," he writes. "A few bees land on a nearby branch, expose their scent glands located near the tip of the abdomen, fan their wings and blow air over the sponge-like gland spreading a chemical scent through the air. The chemical smells like citrus and attracts the other bees flying in the swarm to land on the branch. The queen alights, and soon the swarm is hanging, locked together foot to foot to body in a football-shaped mass, the swarm cluster. This is an intermediate rendezvous point, a place for a temporary bivouac from which the scouts can operate and find a new, permanent home. Some bees initiate foraging, bringing back supplies to feed the masses, while the scouts branch out and scout the landscape looking for the perfect nest site. The scouts are part hunter, part surveyor and part engineer."
Honey bees are both artists and engineers, Page writes in his book. As environmental artists, bees are "responsible for the brilliantly colored flowers in our landscapes," and as environmental engineers, they engineer “the niches of multitudes of plants, animals and microbes."
But back to the bee swarm at the Starner home.
Starner contacted a Vacaville beekeeping family, Craig and Shelly Hunt and daughters Alyssa, 13 and Emma, 8. They arrived in the early evening, around 6, to collect the bees. Before the COVID-19 pandemic hit, Craig taught 4-H'ers (including Alyssa and Emma) the art of beekeeping.
"It was a huge swarm," Shelly said. "We filled two boxes."
The bees are now thriving in the Hunt family's apiary on Meridian Road.
It's bees-ness as usual for the Hunts.
And home, sweet home for the bees.
Have you ever pulled up a chair in your garden and watched honey bees foraging?
They are so intent on their "bees-ness" that they don't know you're there. It's a great opportunity to photograph them.
Sometimes, if you're lucky, they'll buzz over your head on their way back to their colony, and you'll see:
- The three main body parts: head, thorax and abdomen
- The two pairs of wings
- The three pairs of legs
- The pair of antennae
Such was the case in Vacaville this week when we were watching honey bees forage in our African blue basil, a bee magnet that we plant annually. We first learned of African blue basil, (Ocimum kilimandscharicum × basilicum 'Dark Opal'), through Gordon Frankie, UC Berkeley professor and the late Robbin Thorp, distinguished emeritus professor of entomology at UC Davis. They co-authored the book, California Bees and Blooms: a Guide for Gardeners and Naturalists (Heyday Books) with Rollin Coville and Barbara Ertter, also affiliated with UC Berkeley.
Want to know more about honey bees? Be sure to read the newly published The Art of the Honey Bee; Shaping the Environment from Landscapes to Societies (Oxford University Press) by noted bee geneticist and biologist Robert E. Page Jr., who maintains strong ties to UC Davis and Arizona State University (ASU). Also learn about honey bee anatomy on ASU's web page, "Ask a Biologist."
Page, who holds a doctorate in entomology from UC Davis, is a former chair of the UC Davis Department of Entomology. In 2004, Arizona State University (ASU) recruited him for what would become a series of top-level administrative roles. He advanced from director of the School of Life Sciences to dean of Life Sciences; vice provost and dean of the College of Liberal Arts and Sciences; and university provost. Today he holds the titles of provost emeritus of ASU and Regents professor emeritus, as well as UC Davis department chair emeritus, professor emeritus, and UC Davis distinguished emeritus professor.
Did you know a bee has a tool kit? Page lists the tool kit in his book, The Art of the Bee: a compass, an odometer and a path integrator.
'As 'central place foragers,' bees fly out from the nest site and explore the surrounding environment in search of food resources," writes Page, renowned for his research on honey bee behavior and population genetics, particularly the evolution of complex social behavior. "They return to the nest with the resources they collect. To do this, they need to be able to navigate out and find their way back. To aid them, they have a toolkit of navigation mechanisms."
One tool in their tool kit is their internal compass that depends on the location of the sun.
"As light from the sun passes through the atmosphere, it becomes polarized," Page writes. "The pattern of polarized light in the sky depends on the angle of the sun relative to where you are looking. Bees have special sensors in their eyes for detecting the polarized light patterns. On cloudy days, they can't see the sky; but they can still locate the sun using ultraviolet light detectors. Ultraviolet light penetrates cloud cover, allowing bees to use the location of the sun as a navigational marker. With heavy clouds, bees can get to and from a resource by relying solely on landmarks that they learn; otherwise, they stay home until the weather changes. However, as the earth turns, the sun is always changing location relative to the horizon, making it an unreliable marker unless you know the time of day, and bees do. They learn the movement of the sun across the sky and reference it to an internal clock. We know they have the clock because we can train them to forage at specific times of day. If you anesthetize a bee, you can stop her clock. When she awakens and takes a foraging trip to a learned foraging station, her flight path will be offset by the amount of time lost. In other words, she will misinterpret the direction based on the current location of the sun by the amount of time she was anesthetized."
"The odometer plus the ability to determine a flight vector (direction and distance) from a given landmark along a resource flight path, using their sun compass and internal clock, give bees the basic tools for navigation," Page writes. "The last tool in the toolkit is a path integrator that combines the compass and odometer information."
It's a fascinating book by Page, whose most salient contributions to science include constructing the first genomic map of the honey bee, which sparked a variety of pioneering contributions not only to insect biology but to genetics at large.
Meanwhile, take the challenge. Pull up a chair in your garden and watch and photograph the bees going about their "bees-ness."
Caroline Yelle, 28, owner of Pope Canyon Queens (PCQ) at 8307 Quail Canyon Road Quail Canyon Road, Vacaville, lost her business when the lightning-sparked Hennessey Fire, part of the LNU Lightning Complex Fire, swept through rural Vacaville on Aug. 19 from Napa County.
The raging wall of flame "destroyed everything."
She has nothing left but hope.
Pope Valley Queens is one of the nation's few women-owned queen bee breeder businesses. Yelle breeds bees for "a better tomorrow" and now "tomorrow" and "better" are almost singed from her vocabulary.
She lost 500 hives.
Her mentor, best friend and business partner Rick Schubert (who recently sold his business, Bee Happy Apiary, Vacaville), lost everything in the Hennessey Fire, including his newly remodeled home at 8307 Quail Canyon Road--and where the PCQ office was.
"I bought the company in 2017 from my mentor," said Yelle, who began working there in 2012. "This year, 2020 is my seventh year in producing queens."
"I was studying to be a lawyer in Canada," she related. "After I got my degree, I decided to move here and left everything behind to follow my dream with the bees and helping them."
Veteran beekeeper Schubert, who has kept bees for some four decades, is well known in the bee industry and agricultural world. He helped her settle in California and build the company, offering contacts and expertise. "Rick had just remodeled his house and that (the fire) happened," Yelle said. "He lost everything." Schubert's only surviving bees are the 100 hives he keeps in Dixon.
"Basically after selling Bee Happy, he invested in my company, Pope Canyon Queens," she said. "We lost everything together on different levels."
We Lost the Farm
"We (Rick Schubert and her) lost the farm, the house, the garage, the bees," Yelle said. "We have the majority of our bees on another property up in Pope Canyon Valley that also burned. We lost around 500 hives or $100,000 in livestock--minimum--that is not covered...and another $100,000 of benefits out of these hives. We are back to ground zero."
Yelle mainly breeds Carniolans, Apis mellifera carnica, a subspecies of the western honey bee and "a hybrid that we selected in Canada and we reproduce here in California for stronger genes."
"The Canadian beekeeping industry needs tons of early queens in the spring," she said. "We decided seven years ago to bring our northern and robust queen bee genetics, selected over more than 20 years, to produce here." She has an isolated mating station in Napa Valley (Pope Canyon Valley).
"Our goal was not to compete with the big queen guys that already export massive amount of queens but try to increase the level of quality standard into the queen importation issue in Canada and the United States," Yelle said. Over the years, they reached their goal of quality standard.
"However," she said, "we are still working to improve our genetics and to expand our production year after year."
Bee Source published this about the business in 2017: "Pope Canyon Queens LLC (PCQ) want and choose to be at the forefront breeding genetics to help bee populations to better defend themselves against mites, viruses, bacteria, pollination and commercial beekeeping stresses, pollution, depleting floral diversity and ever changing ecosystems. By confronting these challenges head on, PCQ will come to represent a turning point in the strengthening of bee populations. Its 'raison d'etre' is rooted in the urgency of grafting solid apicultural know-how onto strong genetics to meet today's challenge of breeding a better tomorrow."
'It Will Take Years to Recover'
Bee breeder-geneticist Susan Cobey of Washington State University, a former manager of the Harry H. Laidlaw Jr. Honey Bee Research Facility at UC Davis, called the fire "devastating." She knows of several beekeepers, including the Yelle-Schubert team, who lost everything in the tragic fire. "It will take years to recover."
"The story needs to be told," said Cobey, who breeds Carniolans. "These beekeepers work so hard. The impact of California agriculture will be huge, our breadbasket. It's about climate change, too."
"Sue is part of our family group," Yelle said. "We had programs on breeding stock and selection of genes." Yelle also works closely with bee breeder-geneticist Kim Fondrk, of the Laidlaw facility. For decades, Fondrk managed research bee colonies at the Laidlaw facility for Robert Page Jr., former chair of the UC Davis Department of Entomology who recently retired as provost at Arizona State University. Together Page and Fondrk wrote landmark research articles.
"Kim worked with and for us for us over the past years," Yelle recalled. Schubert also worked with bee scientist Norm Gary, emeritus professor, UC Davis Department of Entomology and Nematology, also known as an author, bee wrangler and musician. "We provided bees for Norm's research," Yelle related. Schubert provided bees for Gary's bee wrangling projects.
Now Yelle, who is accustomed to helping others, needs others' help.
"We need help with the bees that burned to be able to keep breeding them and bring back our livestock for next year pollination and to keep feeding the nation," Yelle said.
Yelle has set up a gofundme account, "Help Us Rebuild to Save the Bees," at https://gf.me/u/ys2vtw
"The help and support we are getting is really heartwarming," Yelle wrote on on the gofundme support page. "Thank you for the messages, the calls, the shares, the donations, the thoughts and everything. I see every single of your names and have such strong emotions about how much people care about us, about the bees and about their community. Some really good news so far: a bee company contacted us to help us rebuild the materials for lowest cost possible, my California family offered me a part of their barn for me to have a start before rebuilding."
Yelle is grateful that "someone saved a bee yard that was literally in the middle of one of the worst part of the fire," and she and a neighbor helped saved a mini farm from the fire. "Community is strong."
Strong...and from heartbreaking to heartwarming...