The Chemical Ecology of Lemur Seed Dispersal

• Applicant: Dr. Omer Nevo
• Subject Area: Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions ; Evolution, Anthropology ; Ecology and Biodiversity of Plants and Ecosystems
• Term: from 2016 to 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 318535146

• Final Report Year: 2022

Final Report Abstract

Fleshy fruits have evolved to be attractive to frugivores (fruit eating animals) who consume them and dispersed their seeds. Frugivores differ in their physiological, behavioral, and sensory capacities. This exerts selective pressures on fruit traits, and has been hypothesized to be the major driver behind the tremendous diversity of fruit traits found in the wild. Non-human primates, our closest living relatives, are one of the most important vectors of seed dispersal in the tropics. Having long been seen as having low olfactory capacities, it is now widely acknowledged that they possess an excellent sense of smell that is particularly tuned towards the scent of ripe fruits. This leads to the possibility that fruit scent has evolved as a communication system between primates and plants they consume. The project, conducted between 2016 - 2021, tested this hypothesis in a model system in Madagascar, where most plants rely on dispersal by the island’s endemic primates - the lemurs, whereas a minority relies on dispersal by birds. Lemurs tend to be red-green color blind and some of them are night active, while frugivorous birds tend to have an excellent color vision, are day active, and tend to rely less on their sense of smell. The research showed that plants that have evolved to rely on lemurs for seed dispersal tend to signal the ripeness of their fruits by changing their chemical composition, and that lemurs use this information to infer fruit quality. The study also found that some chemicals in fruit scent may inform animals about fruit nutrient content. Another aspect of the research compared fruits in Madagascar to communities in continental Africa, where frugivorous birds are much more common, and where local primates are not red-green color blind. It found that fruit color is also shaped by frugivore senses: fruits in Madagascar tend to be less red, presumably because there are fewer frugivores who can perceive it. But at the same time, fruits in Madagascar tend to invest more in colors that are salient to red-green colorblind animals. Taken together, these results laid support to the hypothesis that animal senses play a significant force in shaping fruit traits like color and scent, and have played a major role in bringing about the tremendous diversity of wild fruits worldwide. Given that all domesticated human-consumed fruits derive from wild relatives, these results help explain how the diverse pool of fruits available for domestication came to be, and what maintains this diversity. These results drew considerable media attention, being highlighted in venues such as the New York Times, ABC news, NPR, SWP, CBC, and Discover Magazine.

Publications

• (2017). Fruit defence syndromes: the independent evolution of mechanical and chemical defences. Evolutionary Ecology, 31, 913–923
  Nevo, O., Valenta, K., Tevlin, A. G., Omeja, P., Styler, S. A., Jackson, D. J., … Ayasse, M.
  
• (2017). Plant attractants: integrating insights from pollination and seed dispersal ecology. Evolutionary Ecology, 31(2), 249–267
  Valenta, K., Nevo, O., Martel, C., & Chapman, C. A.
  
• (2018). Frugivores and the evolution of fruit colour. Biology Letters, 14, 20180377
  Nevo, O., Valenta, K., Razafimandimby, D., Melin, A. D., Ayasse, M., & Chapman, C. A.
  
• (2018). Fruit scent as an evolved signal to primate seed dispersal. Science Advances, 4, eaat4871
  Nevo, O., Razafimandimby, D., Jeffrey, J. A. J., Schulz, S., & Ayasse, M.
  
• (2018). The evolution of fruit colour: phylogeny, abiotic factors and the role of mutualists. Scientific Reports, 8, 14302
  Valenta, K., Kalbitzer, U., Razafimandimby, D., Omeja, P., Ayasse, M., Chapman, C. A., & Nevo, O.
  
• 2019. Fruit scent and observer color vision shape food-selection strategies by wild capuchin monkeys. Nature Communications 10: 2407
  Melin AD, Nevo O, Shirasu M, Williamson R, Garrett E, Endo M, Sakurai K, Matsushida Y, Touhara K, Kawamura S
  
• 2019. Signal and reward in wild fleshy fruits: Does fruit scent predict nutrient content? Ecology and Evolution 9: 10534-10543
  Nevo O, Razafimandimby D, Valenta K, Jeffrey JAJ, Reisdorff C, Chapman CA, Ganzhorn JU, Ayasse M
  
• 2020. The dispersal syndrome hypothesis: how animals shaped fruit traits, and how they did not. Invited review, Functional Ecology 34: 1159-1168
  Valenta K, Nevo O.
  
• 2020. The evolution of fruit scent: phylogenetic and developmental constraints. BMC Evolutionary Biology 20
  Nevo O, Valenta K, Kleiner A, Razafimandimby D, Jeffery JAJ, Chapman CA, Ayasse M
  
• 2022. Variation in fruit hardness: a mechanical constraint? Oikos
  Valenta K, Brhamdat HD, Calhoun GV, Daegling DJ, Nevo O