The evolution of social behavior

Kocher Lab @ Princeton

Overview

Social species are often wildly successful in nature, but group living is difficult to achieve and maintain.

In the Kocher Lab, we are interested in understanding how and why social behavior evolves. We study systems that have extensive variation in social behavior, and use complementary approaches from population and quantitative genetics through field ecology and mathematical modeling to understand how genes and ecology interact to shape social traits.

We are always looking for talented scientists to join our group. If interested, send us an email.

PROJECTS

We study the forces driving variation in social behavior across multiple levels of biological organization, from molecular and physiological mechanisms underlying individual behavior to the ecological and genetic mechanisms influencing social evolution.

Click on the links above to learn more about some of our projects.


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Does selection act on similar pathways to shape social evolution?

Halictid bees exhibit remarkable diversity in social behavior, both within and between species. Within this family, social behavior has twice evolved independently. There have also been many replicated losses of sociality in this group, making halictid bees some of the most behaviorally diverse social insects on the planet.

The repeated gains and losses of social behavior in halictids create a powerful framework for a comparative approach. Through genomic comparisons, we can ask if selection has acted on the same or similar molecular pathways to shape social traits in this group. We are currently in the process of sequencing the genomes of taxa that represent all of the major gains and losses of social behavior in this family.

RELEVANT PUBLICATIONS

• Kocher, S. D., & Paxton, R. J. (2014). Comparative methods offer powerful insights into social evolution in bees. Apidologie, 1–17–17.
• Kapheim, K. M., Pan, H., Li, C., Salzberg, S. L., Puiu, D., Magoc, T., et al. (2015). Genomic signatures of evolutionary transitions from solitary to group living. Science, 348(6239), 1139–1143.

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Phylogeny from: Gibbs, J., Brady, S. G., Kanda, K., & Danforth, B. N. (2012). Phylogeny of halictine bees supports a shared origin of eusociality for Halictus and Lasioglossum (Apoidea: Anthophila: Halictidae). Mol Phylogenet Evol, 65(3), 926–939.

The genetic basis of a social polymorphism

Taxa that harbor natural phenotypic variation are ideal for studying how the interplay between genetic and environmental factors can lead to the evolution of complex traits.

The social structure of the halictid bee, Lasioglossum albipes, varies among populations: some are solitary, others are social. Common garden experiments established that this behavioral polymorphism is likely to have a strong genetic component. This enables the application of genomic tools to elucidate the genetic basis of sociality and to investigate how environmental cues act on these genes to produce the observed variation. We are using population genomics to characterize the genes and alleles underlying the social polymorphism in this species.

RELEVANT PUBLICATIONS


Kocher, SD, Mallarino, RM, Rubin, BER, et al (2018) The genetic basis of a social polymorphism in halictid bees. Nature Communications, 9(1), 4338.

Ecological factors influencing social composition of bee communities

Understanding the molecular mechanisms underlying variation in social behavior is only part of the puzzle – environmental factors and species interactions are often driving forces of phenotypic evolution.

Variation in sociality with respect to geographic patterns may give hints to some of the relevant ecological factors shaping this trait. For example, biogeographic patterns in the distribution of social systems in insects vary considerably. However, these patterns are inconsistent – in some taxonomic groups, increasing latitude and altitude is associated with a decrease in social structure, while in other groups, the opposite pattern is observed.

In a study using collection records from Switzerland, we documented a strong, but bimodal, link between altitude and sociality in bees and found that variation in development time between social forms may explain these contrasting patterns. It appears that the local environment has a major impact on the social composition of bee communities, but that the nature of this effect varies depending on the degree of sociality for any given species: less social species tend to be lost in harsh environments, while highly social species are able to cope with a much wider climatic range. This suggests that the evolution of social behavior is most likely to occur in areas with mild environmental conditions, but as groups develop into more integrated societies, they are capable of coping with harsher environmental conditions and can increase their ecological ranges.

We are currently expanding this work to look at ecological correlates of social behavior across a much broader range of species and environmental factors.

RELEVANT PUBLICATIONS

Kocher, S. D., Pellissier, L., Veller, C., Purcell, J., Nowak, M. A., Chapuisat, M., & Pierce, N. E. (2014). Transitions in social complexity along elevational gradients reveal a combined impact of season length and development time on social evolution. Proceedings of the Royal Society of London B: Biological Sciences, 281(1787), 20140627.

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A scalable pipeline to study social interactions

Social behavior is a collective phenotype, where individuals create a whole greater than the sum of its parts. This relationship between individuals and the collective remains an elusive question with implications across biological systems. Social network analysis, where collective behaviors are modeled as a suite of pairwise interactions, is a powerful mathematical model to study these collective behaviors. Bumblebee colonies represent an excellent, perturbable model system for social network analysis, due to their small colony size, well-studied genetics, simple communication networks, and annual life history. As a lab, we have developed a scalable pipeline for analyzing colony-level dynamics to study individual and collective behaviors.

RELEVANT PUBLICATIONS

Crall, JD, Gravish, N, Mountcastle, AM, Kocher, SD, Oppenheimer, RL, Pierce, NE, and Combes, SE. (2018). Spatial fidelity of workers predicts collective response to disturbance in a social insect. Nature Communications 9, 1201.

The evolution of maternal care and communication

Eusociality, with overlapping generations and a non-reproducing worker caste, represents an extreme form of social behavior that extremely successful, but rare and difficult to evolve. In contrast, maternal care is much more common throughout the animal kingdom, and is thought to be an important precursor to the evolution of eusociality.

Many insects exhibit some form of maternal care, whether it be egg-guarding or extended provisioning and defense of their offspring. In the treehoppers, maternal care has originated at least 3 times, and like halictids, there have also been many subsequent reversals. This variation creates statistical independence for comparative studies.

Treehoppers exhibit extreme diversity in a number of additional morphological, behavioral, and ecological traits. And like halictid bees, there is also extensive variation in some of these traits within species, opening the door to quantitative and population genetic approaches.

In collaboration with Rex Cocroft (U Missouri, Columbia), we have generated a panel of inbred lines for Tylopelta gibbera, a species that varies in nymphal social behavior and communication. We are using these lines to conduct quantitative genetic and functional studies aimed at identifying the genetic and physiological mechanisms underlying variation in these traits.



Phylogeny from: Lin, C.-P., Danforth, B. N., & Wood, T. K. (2004). Molecular Phylogenetics and Evolution of Maternal Care in Membracine Treehoppers. Systematic Biology, 53(3), 400–421.

Lab members

Sarah Kocher

Principal Investigator

Sarah integrates methods from many different areas of biology to study the evolution of animal behavior. She was one of the first graduates of the Integrative Biology program at the University of Illinois, Urbana-Champaign where she gained research experience in molecular biology, neuroscience and behavioral ecology. She went on to study the genetic and physiological underpinnings of queen-worker interactions in honey bees as a graduate student at NC State. Later, she wanted to study a group of species that spanned the full range of social forms and began her work on halictid bees at Harvard where she was awarded fellowships from the FQEB program and USDA-NIFA.

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Eli Wyman

Lab Manager

Eli began his foray into the biological sciences as a volunteer at the Belize Botanic Gardens, where he got his very first taste of neotropical biodiversity. Later, he found himself a bit adrift in Costa Rica for “one year”, and he decided to volunteer at a butterfly garden and insect museum. It was here that Eli was first exposed to the science of entomology and he knew right away this would become a major interest in his life. At this time, he was most fascinated by the odd and highly variable pronotums of tropical Membracidae as well as their maternal care behaviors. Eli was quickly offered a managerial position at the gardens, where he stayed for four years, but eventually felt homesick and made his way back to the USA. Keen to continue working with insects, Eli almost magically landed a position at the American Museum of Natural History working with Jerome “Jerry” Rozen and John Ascher, where he remained for four years. Drs. Rozen and Ascher became mentors and inspirations to Eli, and their knowledge and affection for bees became integral to his scientific interests. During that time he learned a great deal about bees and met many researchers working on Hymenoptera, including Dr. Kocher. Seeing a very rare opportunity to work with both membracids and bees while expanding his knowledge of genomics, Eli jumped at the chance to join the Kocher Lab.


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Andrew Webb

Associate Research Scholar

Andrew studied Biotechnology (B.Sc. cum laude) and Genetics (M.Sc.) at UC Davis where his research examined developmental mutations in chickens with Dr. Mary Delany. He joined Dr. Mary O’Connel’s lab for his doctoral studies, where he studied the molecular underpinnings of phenotypic variation in humans and mice. He then joined Jody Hey’s lab at Temple where he developed bioinformatic pipelines to faciltate consistent, standardized population genetic pipelines.


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Nikki van Dorp

Molecular Technician

Nikki received her BSc in Biology and Medical Laboratory Research from University of Applied Science Leiden in the Netherlands. She joined the CUBE lab at the Erasmus MC to help study the way the brain orchestrates motor adaptation and motor learning using functional ultrasound. In the Kocher lab, she is studying the mechanisms that generate variation in social behavior by combining cutting-edge genomic and neurobiological tools with field and lab studies.

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Z. Yan Wang

Postdoc

Yan’s research focuses on the evolutionary neurobiology of social behaviors in invertebrates. She completed her PhD in Dr. Cliff Ragsdale’s lab at the University of Chicago, where she characterized neuroendocrine factors that drive maternal behaviors and death in Octopus bimaculoides. Before that, she studied biology, English literature, and Asian American Studies at Cornell University. In the Kocher Lab, she is excited to investigate the evolution of bee brains and social behaviors.




Beryl Jones

Postdoc

Beryl is broadly interested in the role of phenotypic plasticity in shaping the evolution of novel traits. She is enamored with social insects, and uses a comparative approach to study the molecular underpinnings of social behaviors in bees. She received a B.S. from the University of Arizona before completing her Ph.D. in Dr. Gene Robinson’s lab at the University of Illinois at Urbana-Champaign, where she studied mechanisms of reproductive plasticity in two bee species. In the Kocher lab, she is excited to integrate behavior and ecology with modern molecular techniques across many species of sweat bees, leveraging the impressive diversity of social behaviors in this group to better understand the mechanisms that influence evolutionary gains and losses of social behavior.


Callum Kingwell

Postdoc

Callum is interested in mechanisms of communication and their evolution, and in particular chemical signaling systems which are used extensively by social insects. He completed a B.Sc. (hons.) in Evolutionary Biology at the University of British Columbia, then completed his Ph.D. in Dr. Robert Raguso’s lab in the Department of Neurobiology and Behavior at Cornell University. During his Ph.D. work, Callum characterized the queen pheromones of flexibly social sweat bees in Dr. William Wcislo’s research group at the Smithsonian Tropical Research Institute in Panama. In the Kocher lab, he plans to leverage new techniques and a comparative approach across the sweat bee phylogeny to better understand the molecular underpinnings of pheromonal signals and their importance for social evolution.


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Ian Traniello

Lewis-Sigler Scholar

Ian is interested in the evolution and maintenance of social organization, beginning with the fundamental question of how a brain “wired” for solitary life can handle the intense push-and-pull of group living. In the Kocher Lab, he explores the neurogenomic architecture of collective and individual behaviors, focusing on molecular correlates of gains and losses of sociality in bees. This focus is subserved by cutting-edge sequencing technologies like single-cell and spatial ‘omics, platforms and analytical pipelines Ian is developing and adapting for bees through close collaboration with the Pritykin Lab at LSI. Ian studied neuroscience and physiology in the Collaborative Degree Program at Boston University, where he earned his joint BS/BA degrees before completing his Neuroscience PhD in Dr. Gene E. Robinson’s lab at the University of Illinois at Urbana-Champaign. Outside of lab, he has over half a decade of experience teaching STEM to incarcerated students, and he is passionate about using science education to build community and create a world without prisons.


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Micah Fletcher

QCB Grad Student

Micah is a PhD student in the Quantitative and Computational Biology program, whose research focuses on the evolution of behavior in treehoppers, a family of hemipteran insects that have gained and lost both maternal care and honeydew-for-protection mutualism with ants multiple times. He earned his B.S. from the University of Missouri – Columbia studying the mechanisms male-male competitive signaling during male-female mate searching duets in treehoppers using plant-borne vibration playback experiments under the direction of Rex Cocroft. Since joining the Kocher Lab, he has been using field experiments, comparative genomics and comparative phylogenetic methods to study how life history and ant mutualism have shaped the evolution of maternal care in treehoppers.


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Dee Ruttenberg

QCB Grad Student

Dee received a BS in Biological Sciences (specializing in genetics) at the University of Chicago. They completed their undergraduate thesis with Dr. Marcus Kronforst on Elymnias hypermnestra, a Batesian mimic whose model varies across a geographic mosaic in Southeast Asia. Using computational genomics, Dee found the genetic factors that underlie E. hypermnestra’s mimicry. It was Dee’s experience taking linguistics courses at UChicago, however, that got them interested in the biology behind communication. As a PhD Student in Quantitative and Computational Biology at Princeton, they are integrating computer vision, genomic, and ecological techniques to better understand how bumblebees make and remake a communication network year after year. This project is currently funded by a NSF GRFP grant. Outside of lab, they love teaching, board games, hiking, Commedia dell’arte, and collecting tchotchke turtles (Chelonia tchotchkeus, seen to the right).


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Kennedy Saitoti

EEB Grad Student

Kennedy received his B.S in Biology from University of Nairobi in Kenya. He has an ardent love for insects and has a particular interest in behavior, evolution, and genomics. He found his passion for ecology and evolution while working with researchers studying the African Queen butterfly at the Mpala Research Centre in Kenya. As a graduate student in the Kocher Lab, he is studying the interplay of genes and the environment in regulating and shaping the behavior and physiology of halictid bees.



Undergraduate Researchers
Lila Harmar

EEB, Class of 2022


Tatum Gee

EEB, Class of 2022


Alexis Kane

EEB, Class of 2022


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Daniel Knapp

Physics, Class of 2023


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Publications

google scholarSelected Publications:

  • Jones, BM, Rubin, BER, Dudchenko, O, Kapheim, KM, Wyman, ES, St. Hillaire, BG, Liu, W, Parsons, LP, Jackson, SR, Goodwin, K, Davidson, SM, Kingwell, CJ, Webb, AE, Fernández Otárola, M, Pham, M, Omer, AD, Weisz, D, Schraiber, J, Villanea, F, Wcislo, WT, Paxton, RJ, Hunt, BG, Aiden, EL, Kocher, SD (2021). Convergent selection on hormone signaling is associated with the evolution of eusociality in bees. bioRxiv 2021.04.14.439731.
  • Pereira, TD, Tabris, N, Li, J, Ravindranath, S, Papadoyannis, ES, Wang, ZY, Turner, DM, McKenzie-Smith, G, Kocher, SD, Falkner, AL, Shaevitz, JW, Murthy, M. (2020). SLEAP: Multi-animal pose tracking. bioRxiv 2020.08.31.276246.
  • Rubin, BER, Jones, BM, Hunt, BG, and Kocher, SD (2019). Rate variation in the evolution of non-coding DNA associated with social evolution in bees. Phil. Trans. R. Soc. B 374:20180247.
  • Rubin, BER, Jones, BM, Hunt, BG, and Kocher, SD (2019). Rozen, JG, Smith, CS, Kocher, SD, Wyman, ES (2018). Developmental biology among corbiculate bees: Bombus impatiens, including observations on its egg eclosion. American Museum Novitates 3912:1-27.
  • Kocher, SD, Mallarino, RM, Rubin, BER, Yu, DW, Hoekstra, HE, and Pierce, NE (2018). The genetic basis of a social polymorphism in halictid bees. Nature Communications 9 (1), 4338.
  • Rubin, BER, Sanders, JG, Turner, KM, Pierce, NE and Kocher, SD (2018). Social behaviour in bees influences the abundance of Sodalis (Enterobacteriaceae) symbionts. Royal Society Open Science, 5 (7), 180369.
  • Crall, JD, Gravish, N, Mountcastle, AM, Kocher, SD, Oppenheimer, RL, Pierce, NE, and Combes, SE (2018). Spatial fidelity of workers predicts collective response to disturbance in a social insect. Nature Communications 9, 1201.
  • Galbraith, DA, Fuller, ZL, Ray, AM, Brockmann, A, Frazier, M, Gikungu, MW, Iturralde Martinez, JF, Kapheim, KM, Kerby, JT, Kocher, SD, Losyev, O, Muli, E, Patch, HM, Rosa, C, Sakamoto, JM, Stanley, S, Vaudo, AD, and Grozinger, CM (2018). Investigating the viral ecology of global bee communities with high-throughput metagenomics. Scientific Reports 1: 8879.
  • Glastad, KM, Arsenault, SV, Vertacnik, KL, Geib, SM, Kay, S, Danforth, BN, Rehan, SM, Linnen, CR, Kocher, SD*, Hunt, BG* (2017). Variation in DNA methylation is not consistently reflected by sociality in Hymenoptera. Genome Biol Evol, evx128. *co-corresponding
  • Wittwer, BW, Hefetz, A, Simon, T, Murphy, LEK, Elgar, MA, Pierce, NE, and Kocher, SD (2017). Solitary bees reduce investment in communication compared with their social relatives. PNAS, 114(25): 6569-6574.
  • Engel, P, Kwong, W, McFrederick, Q, Anderson, et al. (2016). The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions. mBio 7 (2), e02164-15.
  • Galbraith, DA, Kocher, SD, Glenn, T, Albert, I, Hunt, GJ, Strassmann, JE, Queller, DC and Grozinger, CM (2016). Testing the kinship theory of intragenomic conflict in honey bees (Apis mellifera). PNAS, 201516636.
  • Kapheim KM, Pan H, Li C, et al. (2015). Genomic signatures of evolutionary transitions from solitary to group living. Science348(6239), 1139-1143.
  • Kocher, SD, Tsuruda, JM, Gibson, JD, Emore, CM, Arechavaleta-Velasco, ME, Queller, DC, Strassmann, JE, Grozinger, CM, Gribskov, MR, San Miguel, P, and Westerman, R (2015). A search for parent-of-origin effects on honey bee gene expression. G3: Genes| Genomes| Genetics5(8), 1657-1662.
  • Fu, F, Kocher, SD, Nowak, MA (2014). The risk-return tradeoff between solitary and eusocial reproduction. Ecology Letters, 18(1), 74-84.
  • Kocher, SD, Pellissier, L, Veller, C, Purcell, J, Nowak, M, Chapuisat, M, and Pierce, NE. (2014). Transitions in social complexity along altitudinal gradients reveal a dual impact of climate on social evolution. Proc Roy Soc B. 281 (1787): 20140627.
  • Kocher, SD and Paxton, RJ. (2014). Comparative methods offer powerful insights into social evolution. Invited review, Apidologie, 45(3): 289-305.
  • Kocher, SD, Li, C, Yang, W, Tan, H, Yi, SV, Yang, X, Hoekstra, HE, Zhang, G, Pierce, NE, Yu, DW. (2013). The genome of a socially polymorphic halictid bee, Lasioglossum albipes. Genome Biology 14(12):R142.