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.

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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 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

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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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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.


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Paul Davison

Postdoc

Paul received a Masters in Zoology from Bangor University in North Wales. There he completed research projects on ecological speciation of geckos in the Canary Islands, and the spatial distribution of honeybee mating aggregations. Studying honeybees spurned an interest in the origins of complex social behavior, and in particular the processes driving the transition from solitary to social living. To pursue his interests further Paul moved to the University of Sussex and completed a PhD with Professor Jeremy Field, where he focused on the mechanisms underlying social polymorphism in sweat bees. Having acquired a keen interest in sweat bees, he joined the Kocher lab as a postdoc and now utilizes laboratory-reared bees to investigate the environmental and genetic processes that shape sweat bee social behavior.


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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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Serge Picard

Research Associate

Serge received his BS in Biochemistry from UQTR (Université du Québec à Trois-Rivières) and a Grad diploma in Bioinformatics from UQAM (Université du Québec à Montréal). He began his career in Endocrinology focusing on hypertension in pregnancy at the Centre Hospitalier Universitaire Sainte-Justine. He then switched to immunology working on host response to Candida albicans and the development of immunodominant antigens for immunotherapeutic cancer treatment at the Biotechnology Research Institute of Montreal. He then moved on to Next Gen Sequencing providing innovative library prep and sequencing solutions for a variety of assays and organisms for Janelia Research Campus and Princeton University where he collaborates with the Andolfatto, Ayroles, and Kocher labs.


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Erin Lowe

Research Specialist

Erin received her B.A. in Biology and Environmental Studies from Swarthmore College in 2014. She is passionate about pollinators and has worked on research projects ranging from pollinator phenology in the Rocky Mountains to the influence of dominance in mediating the relationship between biodiversity-ecosystem function for wild bees in New Jersey. She is interested in pollinator diversity and behavior, and is excited to learn more about the processes shaping the social behavior of halictid bees and membracids in the Kocher lab.


Publications

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  • 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.
  • Kocher, SD and Grozinger, CM. (2011). Cooperation, conflict, and the evolution of queen pheromones. Journal of Chemical Ecology, 37(11): 1263-75. *Reviewed in F1000
  • Wang, Y., Kocher, SD, Linksvayer, TA, Grozinger, CM, Page, RE, and Amdam, GV. (2011). Regulation of behaviorally-associated gene networks in worker honey bee ovaries. Journal of Experimental Biology, 215(1): 124-134.
  • Chan QWT, Mutti NS, Foster LJ, Kocher SD, Amdam GV, Wolschin, F. (2011). The worker honeybee fat body proteome is extensively remodeled preceding a major life-history transition. PLoS ONE 6(9): e24794.
  • Kocher, SD, Ayroles, JF, Stone, EA, and Grozinger, CM. (2010). Natural variation in pheromone response correlates with reproductive traits and brain gene expression in worker honey bees. PLoS ONE 5(2): e9116.
  • Kocher, SD, Tarpy, DR, and Grozinger, CM. (2010). The effects of mating and instrumental insemination on honey bee flight behavior and gene expression. Insect Molecular Biology, 19(2): 153-162.
  • Kocher, SD, Richard, FJ, Tarpy, DR, and Grozinger, CM. (2009). Mating induces changes in honey bee queen mandibular gland profiles and ovary development. Behavioral Ecology, 20(5): 1007-1014.
  • Kocher, SD, Richard, FJ, Tarpy, DR, and Grozinger, CM. (2008). Genomic analysis of post-mating changes in the honey bee queen (Apis mellifera). BMC Genomics, 9:232.