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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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, S. D., Li, C., Yang, W., Tan, H., Yi, S. V., Yang, X., et al. (2013). The draft genome of a socially polymorphic halictid bee, Lasioglossum albipes. Genome Biology, 14(12), R142.

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 recent 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.

altitude

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 evolved independently 2-3 times. 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 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.

Email CV

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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Jethary Rader

Molecular Technician

Jethary received a B.A. in biology at Reed College in Portland, Oregon where they wrote their undergraduate thesis on enteropathogenic Escherichia coli (EPEC), which examined the affects of altering different environmental conditions found where EPEC colonizes in the small intestine, in order to see if the changes influenced EPEC pathogenicity. Jethary’s biology interests include pathology and epigenetics. When not in the lab, Jethary is a classical pianist and a NYC model.



Ben Rubin

Postdoc

As an undergraduate at Cornell University, Ben’s very first research experiences focused on the behavioral ecology of birds. All the while, and unbeknownst to him, a passionate love for social Hymenoptera was growing within. So when offered the chance to study the population structure of a mutualistic acacia-ant in Kenya under Professor Irby Lovette, he jumped at the chance, beginning his foray into molecular biology and the power of DNA analysis by developing novel microsatellites. This experience fortified his love of Hymenoptera, and, rediscovering a delight for programming not felt since a high school computer science class, Ben completed a PhD on acacia-ant behavioral genomics at the University of Chicago under Field Museum Curator Corrie Moreau. With the purpose of life now clearly defined, he began a postdoc in the Kocher lab using genomics to study a number of aspects of sweat bee biology. Although nearly any use of non-model genomics can now pique Ben’s interest, he focuses on genome evolution, behavioral genomics, and endosymbiont communities. See more at benrubinbiology.com.


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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.


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.




Dee Ruttenberg

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 hope to combine tools from molecular biology, the computational sciences, and ecology to better understand communication and social behavior in the light of evolution. 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

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.



Micah Fletcher

Grad Student

Micah received his B.S. in biology at the University of Missouri, where he conducted playback experiments to probe male competitive mate-searching interactions in a duetting insect that uses plant-borne vibrations to communicate. He is interested in using computational approaches to answer questions about communication and sociality. He loves listening to podcasts, playing ultimate frisbee, photographing and collecting insects, and nerding out about linguistics and animal behavior.


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Undergraduate Researchers
Karissa Lowe

Karissa is a current undergraduate at Princeton University. She has a keen interest in agriculture and food production services and therefore, pollination. For her senior thesis, Karissa is exploring the use of the solitary bee, Osmia lignaria, on strawberry pollination in indoor vertical farm systems under Sarah Kocher and Paul Gauthier.



Jean Cho

Jean is an undergraduate student at Princeton University. She is interested in the genetic and environmental factors that influence early development and is conducting her thesis research on bumblebee brain development in the Kocher Lab.



Publications

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Selected Publications:

  • 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.
  • 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.