Japan Society for the Promotion of Science

35th Recipient (2019)

Recipient

The Committee on the International Prize for Biology of Japan Society
for the Promotion of Science awards the 2019 International Prize for Biology
in the field of "Biology of Insects" to
Dr. Naomi E. Pierce, Hessel Professor of Biology, Harvard University,

On August 2, the Committee on the International Prize for Biology (chaired by Dr. Hiroo Imura, Vice President, the Japan Academy) decided to award the 35th (2019) International Prize for Biology to Dr. Naomi Ellen Pierce, Hessel Professor of Biology, Harvard University, USA. This year’s Prize is awarded in the field of the Biology of Insects.
Photo of Naomi Ellen Pierce

Naomi Ellen Pierce

Education and Professional Positions

1983                     Ph.D. in Biology, Harvard University
1983–1984        Postdoctoral Fellow, Griffith University
1984–1986        Research Lecturer in Biology, University of Oxford
1986–1989        Assistant Professor, Department of Biology, Princeton University
1989–1990        Associate Professor, Department of Biology, Princeton University
1991–present  Hessel Professor of Biology, Harvard University; Curator of Lepidoptera, Museum of Comparative Zoology

Awards and Distinctions

1988–1993  MacArthur Fellowship
1996               Senior Fellow, Harvard Society of Fellows
2008               Fellow, American Association for the Advancement of Science
2011               Fellow, Entomological Society of America
2012               Honorary Fellow, Royal Entomological Society (UK)
2016               E.O. Wilson Naturalist Award, American Society of Naturalists
2017               Verrill Medal, Peabody Museum, Yale University
2018               Fellow, American Academy of Arts and Sciences

Research Achievements

Evolution of interspecific symbiosis
Dr. Pierce’s research career began with studies of the mutualism between lycaenid larvae and their attendant ants. Dr. Pierce used a variety of experimental approaches to conclude that the behavior of both ants and lycaenid larvae is motivated by self-interest. Lycaenid larvae provide ants with nutritive secretions in exchange for protection against parasitic wasps and other predators. This arrangement comes with a cost to the participants: the larvae, for example, make metabolic sacrifices in order to maintain their ant guard. Given the predominance of self-interest, it is perhaps not surprising that a mutually beneficial relationship can shift to being an exploitative one. Dr. Pierce discovered that when placed in a group, each individual larva will “conserve” its secretions by producing less than it would on its own. Moreover, she established that parasitic behaviors such as those of the caterpillars of certain lycaenid butterflies in the genus Phengaris, whose caterpillars devour ant larvae, have developed numerous times out of mutually beneficial symbioses. Recently, she discovered that lycaenid larvae may use their secretions to manipulate directly dopamine levels in the ants’ brains, with the result that the ants become slavishly devoted caterpillar guards. Contrary to conventional wisdom in the field of life history evolution, she has concluded that parasitism is not necessarily an evolutionary dead-end, with, for example, the Miletinae subfamily of lycaenid butterflies having differentiated into many varieties while remaining either parasitic on ants or carnivorous on insects associated with ants.

Coevolution of ants and gut bacteria
It is estimated that over 20,000 ant species exist today. Dr. Pierce has provided evidence that this evolutionary and ecological success is in part a function of the symbiotic bacteria in their guts. In tropical forest canopies, where ants consume nectar almost exclusively and are therefore chronically in need of protein, Dr. Pierce found that ants have symbiotic gut microbes that recycle nitrogen. That this association has arisen independently in several large clades of arboreal, herbivorous ants is evidence of its adaptive value. She also discovered that there are also numerous bacterial gut symbionts in ants such as army ants that are exclusively carnivorous, and that in contrast to these cases, omnivorous ants tend to have few gut symbionts. Dr. Pierce’s research demonstrates the important role played by “friendly” microbes as organisms venture into extreme environments involving unbalanced diets that are either largely herbivorous or largely carnivorous.

Insect phylogeny and classification
In the contemporary interspecific comparative approach, it is essential to have information about the evolutionary history of the group of organisms under study. Dr. Pierce and her colleagues have created molecular phylogenies of Dr. Pierce’s principal objects of study: butterflies, ants, bees, and the orchids they pollinate. In particular, the overall higher-level phylogenies of ants (Moreau et al. 2006) and butterflies (Espeland et al. 2018) have now become indispensable as standard reference tools. The information they provide supports a variety of theories that reignite past debates on topics such as the Asiatic origins of Polyommatus blue butterflies whose descendants are now found in South America; the role of karyotypes (chromosomes) in driving diversification in Old World relatives of these butterflies; the asynchronous diversification of orchids and their symbiotic bee species; and the communication costs of social evolution for bees.

Molecular biology of insects, plants, and parasitic fungi
In addition to her ecological research outlined above, Dr. Pierce is pursuing research in molecular biology and biochemistry. One of her major successes is in research on the defensive response of plants to two different types of natural threats: herbivore insects and pathogens. This began in studies conducted with colleagues including Harvard Medical School Professor Frederick Ausubel using Arabidopsis (plant) and Pseudomonas (parasitic bacteria) as the two model organisms, but Dr. Pierce’s originality is manifested in the addition of a scaptomyzid leafminer fly that is parasitic in Arabidopsis. This fly is extremely closely related to the model insect Drosophila, and researchers are now using the genomic information of these three organisms to explore the genes and signaling pathways that contribute to the evolution of herbivory by the insects, and defense responses by the plants.

Molecular biology of insect society and visual perception, environmental problems, etc.
Dr. Pierce’s research in molecular biology is also wide-ranging. Apart from the cases noted above, she has succeeded in identifying genes associated with the social behavior of halictid bees, which manifest a number of stages of social development, from solitary to eusocial as well as the opsin genes that contribute to color perception in honeybees and butterflies. Recently she has established that the social behavior of bumblebees is impaired in a number of ways by continued exposure to minute quantities of neonicotinoid insecticides, an achievement that provides insights into “colony collapse syndrome” and the loss of pollinators, as well as the rapid decline of insect biodiversity with its important implications for conservation biology.

Representative Publications and Literatures:

Evolution of symbiotic species interactions
  1. Schär, S., Eastwood, R, Arnaldi, K.G., Talavera, G., Kaliszewska, Z.A., Boyle, J.H., Espeland, M., Nash, D.R., Vila, R. and N.E. Pierce. (2018) Ecological specialization is associated with genetic structure. Proceedings of the Royal Society B 285: 20181158
  2. Hojo, M.K., Pierce, N.E. and K. Tsuji. (2015). Lycaenid caterpillar secretions manipulate attendant ant behavior. Current Biology 25: 2260-2264
  3. Archetti, M., Scheuring, I., Hoffman, M., Frederickson, M.E., Pierce, N.E., Yu, D.W. (2011). Economic game theory for mutualism and cooperation. Ecology Letters 14: 1300-1312 (cover)
  4. Pierce N.E. and P.S. Mead (1981). Parasitoids as selective agents in the symbiosis between lycaenid butterfly caterpillars and ants. Science 211: 1185-1187

Coevolution between ants and microbiota
  1. Hu, Y*, Sanders, J.G. *, Łukasik, P., D’Amelio, K, Millar, J.S., Vann, D.R., Lan, Y., Newton, J.A., Schotanus, M., Kronauer, D.J.C., Pierce, N.E., Moreau, C.S., Wertz, J.T., Engel, P. and J.A. Russell. (2018). Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome. Nature Communications 9: 964
  2. Baker, C.C.M, Martins, D.J., Pelaez, J.N., Billen, J.P.J., Pringle, A., Frederickson, M.E. and N.E. Pierce. (2017) Distinctive fungal communities in an obligate African ant plant mutualism. Proceedings of the Royal Society B 284: 20162501;
  3. Sanders, J.G., Powell, S., Kronauer, D.J.C., Vasconcelos, H.L., Frederickson, M.E. and N.E. Pierce. (2014). Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Molecular Ecology 23: 1268-1283
  4. Russell, J.A., Moreau, C.S., Goldman-Huertas, B., Fujiwara, M., Lohman, D.J. and N.E. Pierce. (2009). Bacterial gut bacteria are tightly linked with the evolution of herbivory in ants. Proceedings of the National Academy of Science USA 106: 21236-21241

Functional analyses of insect/ plant/ microbe interactions
  1. Haney, C.H., Wiesmann, C.L., Shapiro, L.R., O’Sullivan, L. R., Khorasani, S., Melnyk, R.A., Xiao, L. Han, J., Bush, J., Carrillo, J. Pierce, N.E. and F.M. Ausubel. (2018) Rhizosphere-associated Pseudomonas induce systemic resistance to herbivores at the cost of susceptibility to bacterial pathogens. Molecular Ecology 27: 1833-1847
  2. Groen, S.C., Whiteman, N.K., Bahrami, A.K., Wilczek, A.M., Cui, J., Russell, J.A., Cibrian-Jaramillo, A., Butler, I.A.E., Rana, J., Huang, G.H., Bush, J., Ausubel, F.M. and N.E. Pierce. (2013). Pathogen- triggered ethylene signaling mediates systemic induced susceptibility to herbivory in Arabidopsis. Plant Cell 25: 4755-4766
  3. Whiteman, N.K., Gloss, A.D., Sackton, T.B., Groen S.C., Humphrey, P.T., Lapoint, R.T., Sønderby, I.E., Halkier, B.A., Kocks, C., Ausubel, F.M. and N.E. Pierce. (2012). Genes involved in the evolution of herbivory by a leaf-mining, drosophilid fly. Genome Biology and Evolution 4: 900-916 (cover).
  4. Cui, J. Bahrami, A.K., Pringle, E.G., Hernandez-Guzman, G., Bender, C.L., Pierce, N.E. and F. M. Ausubel. (2005). Pseudomonas syringae manipulates systemic plant defense against pathogens and herbivores. Proceedings of the National Academy of Science USA 102: 1791-1796; News & Views, Nature Reviews Microbiology 3: 192

Insect phylogeny and systematics
  1. Espeland, M., Breinholt, J., Willmott, K.R., Warren, A.D., Vila, R., Toussaint, E.F.A., Maunsell, S.C., Kwaku, A.-P.,Talavera, G., Eastwood, R. Jarzyna, M.A., Ries, L. Guralinick, R., Lohman, D.J., Pierce, N. E. and A.Y. Kawahara. (2018). Comprehensive higher-level phylogeny of butterflies (Papilionoidea) inferred from genomic data. Current Biology 28: 770-778
  2. Ramírez, S.R., Eltz, T., Fujiwara, M.K., Gerlach, G., Goldman-Huertas, B., Tsutsui, N.D. and N.E. Pierce. (2011). Asynchronous diversification in a specialized plant-pollinator mutualism. Science 333: 1742-1746
  3. Ramírez, S.R., Gravendeel, B., Singer, R.B., Marshall, C.R. and N.E. Pierce. (2007). Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448: 1042-1045 (cover)
  4. Moreau, C.S., Bell, C.D., Vila, R, Archibald, S.B., and N.E. Pierce. (2006). Phylogeny of the ants: diversification in the age of angiosperms, Science 312: 101-104 (cover)

The evolution of social behavior
  1. Kocher, S.D., Mallarino, R., Rubin, E.R., Yu, D.W, Hoekstra, H.E. and N.E. Pierce (2018) The genetic basis of a social polymorphism in halictid bees. Nature Communications 9: 4338- 4346
  2. Crall, J.D., Switzer, C.M., Oppenheimer, R.L., Ford-Versypt, A., Dey, B., Brown, A., Eyster, M, Guérin, C., Pierce, N.E., Combes, S.A. and B.L. de Bivort. (2018) Chronic neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science 362: 683-386
  3. Wittwer, B., Hefetz, A., Simon, T. Murphy, L.E.K., Elgar, M.A., Pierce, N.E. and S.D. Kocher. (2017) Solitary bees reduce investment in communication compared with their social relatives. Proceedings of the National Academy of Science USA 114: 6569-6574; doi:10.1073/pnas.1620780114 (cover)
  4. Kocher, S.D., Pellissier, L., Veller, C., Purcell, J., Nowak, M.A., Chapuisat, M. and N. E. Pierce. (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 B 281: 20140627.