Collective behaviors are present across many different animal groups: schools of fish swimming in a swirling pattern together, large flocks of birds migrating through the night, groups of bees coordinating their behavior to defend their hive. These behaviors are commonly seen in social insects where as many as thousands of individuals work together, often with distinct roles. In honey bees, the role a bee plays in the colony changes as they age. Younger bees perform duties inside the hive, such as nursing and wax building, while older bees transition to roles outside of the hive, either foraging for food (foragers) or defending the colony (soldiers). What determines whether older bees become foragers or soldiers is unknown, but a new study published in Nature Ecology and Evolution explores the genetic mechanisms underlying the collective behavior of colony defense, and how these mechanisms relate to the colony’s overall aggression.
“Honey bees do not have a size-based division of labor, like you might see in termites or ants,” said Ian Traniello, former graduate student at University of Illinois Urbana-Champaign, now an associate research scholar at Princeton University and first author on the study. “If you ask anyone off the street to guess which ant is a soldier versus a forager, they probably will guess it right 100% of the time, because the soldiers are huge. Honey bees instead have an age-based division of labor, where older bees tend to be foragers or soldiers, both of which are dangerous and potentially lethal roles.” A genome-wide association study conducted previously on a sub-species of honey bee in Puerto Rico that had evolved to be less aggressive in recent years, revealed strong associations between variation in the sequence of some genes and the level of overall colony aggression. Researchers called these “colony aggression genes.” In the current study, researchers compared the expression and regulation of genes in the brains of soldiers and foragers, and across colonies that varied in aggressiveness. Researchers measured colony aggressiveness by counting the number of stings on suede patches placed outside the hives after a disturbance. They identified soldiers as the bees that attacked the patches and foragers as the bees that returned to the hive with pollen. The researchers then used single-cell transcriptomics and gene regulatory network analysis to compare the brains of forager and soldier bees, from low and high aggression colonies. The researchers found that, although there were thousands of genes in the brain that differed in their expression between soldiers and foragers, none of them were part of the colony aggression gene list. However, when they created models of brain gene regulatory networks, which control when and where specific genes are expressed, the researchers found that the structure of these networks differed between soldiers and foragers—and the differences were bigger when the soldiers and foragers came from a more aggressive colony. “What we think is happening is that the regulation of genes associated with collective behavior affects the mechanisms that underlie division of labor,” Traniello explained. “So, colonies can become more or less aggressive by influencing the aggression level of the individuals within that colony. Basically, a forager may be more or less likely to transition to a soldier-like state if the environment calls for it.” The findings highlight the importance of gene regulation to our understanding of the relationship between genes and behavior. “While a few studies have found potential heritable differences between soldiers and foragers, this study demonstrates that older honey bees may have the potential to take on either role,” said Gene Robinson (GNDP), IGB Director and author on the paper. “In colonies that are more aggressive, likely due to increased danger in the environment, older bees may just be more predisposed to become soldiers to help defend the colony.” Plans for future directions include developing functional tests to explore the role of the gene networks identified in the study, and to identify spatially where they are being expressed in the brain. Traniello says that he looks forward to exploring these new questions. “We have extraordinary technologies to probe genes and behavior at an unprecedented scale, both with single-cell and, now, spatial transcriptomics,” Traniello said. “These give us new means for understanding old questions, like the relationship from individual to collective, or the relationship between genotype to phenotype. It’s exciting to be able to take these tools and apply them in naturalistic contexts, and I hope this work inspires others to do the same.” The project was funded by the Illinois Sociogenomics Initiative, and can be found at https://www.nature.com/articles/s41559-023-02090-0.
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Studying behavioral and morphological responses to environmental cues in poison frogs Ask Lisa Surber her thoughts on science and the natural world and you’ll find passion and excitement practically radiate off her as she responds. For Surber, who is currently a 3rd year PhD candidate in the Evolution, Ecology, and Behavior department at University of Illinois Urbana-Champaign, this interest in science and nature has been present within her ever since she was young: “I grew up in Sonoma County in California, and didn't realize what a privilege it was to grow up there until after I moved away,” said Surber. “You get spoiled because you're next to the redwoods, beautiful creeks, and the beaches there too. So, I got a lot of experiences in nature early on.” From her youth, Surber knew she would pursue a career in science, but as she grew she found herself bouncing between different career aspirations, from veterinarian to astronaut to ophthalmologist, to name a few. By the time she was working on her undergraduate degree at Mills College, a small women’s college in California, she was set on becoming a pediatrician. However, she found the enormous amount of learning material daunting, and this experience almost intimidated her away from science. An evolution class in her second year inspired her to keep going, though on a different path than before.
“Learning about evolution was the coolest thing ever!” exclaimed Surber. “I wasn’t really taught about evolution at all in high school, so I didn't understand how connected everything was, and how simple the mechanism of evolution really is. It can lead to these drastic, beautiful adaptations that we can see, and I just love to think now about this beautiful connection we all share.” Later in her undergraduate career, she tried her hand at animal behavior research, studying stress responses in ground squirrels under her mentor, Jennifer Smith. Surber found this research to be rewarding, and so, after graduating, she went for her master’s degree at Sonoma State University under advisors Jeff Wilcox and Derek Girman. Here, she examined movement patterns of California red-legged frogs and invasive bullfrogs. Surber says it was then that Smith, her previous advisor, reached out to her because Eva Fischer (GNDP), a new assistant professor in evolution, ecology, and behavior at Illinois, was starting up a lab that focused on plasticity of behavior in frogs, and she recommended Surber apply there for her PhD. Surber now works in the Fischer lab, studying how dyeing poison frogs detect cues from the environment, and change their behavioral and morphological phenotypes in response to these cues. In this species, the dads will carry and deposit their tadpoles into standing pools of water, and leave them to fend for themselves. “In the wild, there's a lot of variation in the kind of pools that they can be in,” Surber said. “Dads put the tadpole in between logs or plants, basically wherever water can collect. Sometimes they'll be in there by themselves, but then other times they'll have a lot of conspecifics with them.” As such, the tadpoles grow up in a variety of different environments, and cues from these environments may affect their behaviors, as some become increasingly aggressive and cannibalistic towards others. “It really adds drama to the types of phenotypes I measure,” Surber remarked. Specifically, Surber examines the effects of different smells in the water, such as food, conspecifics (member of the same species), and predators. In her experiments thus far, Surber has found that tadpoles reared by themselves grow faster and larger, and survive better during the earlier stages of life than those reared with others. She also found that tadpoles reared alone are more aggressive than tadpoles reared together. Surber says that this plasticity in behavior is a strategy for the frogs. “If you're in a pond with a bunch of other tadpoles, there's a risk to starting a fight,” Surber explained. “They have the same weapons, and could turn around and bite you back. So tadpoles in this environment need to play it cool. But if you were reared by yourself and you're able to grow up faster, then it's beneficial to be aggressive. If another tadpole is introduced into your pool and you attack, then not only are you eliminating a competitor, but then you’re also like ‘thanks for the snack’.” Surber says her projects are now starting to look at mechanisms behind this plasticity, including levels of hormones and neurotransmitters. Her latest project found that tadpoles reared alone also have higher levels of corticosterone, a hormone that mobilizes glucose, and is associated with stress. This hormone is also associated with metamorphosis in frogs, and Surber says high levels of corticosterone in the loner frogs may be what helps them grow faster. In addition to her lab work, Surber says she has many hobbies and pets that keep her life busy and fun, with the word “many” being no exaggeration. Surber loves staying active with weightlifting, judo, boxing, and soccer, and taking her dog Sequoia on long walks. Along with her dog, she also keeps pet cats, turtles, frogs, and fish. Remarking she had almost all of the animal kingdom except for insects and birds, she commented “My best friend Chelsea has a pet bird, so that taxon is covered!” Something Surber is very passionate about is mentoring undergraduates, both when teaching classes and when hiring assistants in her research. The mentoring she received from Smith back when she was an undergraduate inspired her to want to do the same for others. “Smith made such a huge difference in my life, not only in the science that she taught me, but she emphasized that science really is for everybody,” Surber said. “She made me feel so included just by being the goofy and caring woman she is, and I want to be able to do that for other people as well. I want to give back to the community and make sure people have good experiences in science, even if they don’t end up pursuing a career in it. I just want them to remember that science can be fun, and sometimes hard, but mostly fun, and it helps you grow.” Surber hopes to instill this sense of curiosity and excitement about the natural world in all of her students, and states that Sir David Attenborough, her favorite narrator of nature documentaries, said it best: “It seems to me that the natural world is the greatest source of excitement; the greatest source of visual beauty; the greatest source of intellectual interest. It is the greatest source of so much in life that makes life worth living.” |