Olfactory signals are ubiquitous among mammals and serve to advertise quality, reproductive state, and resource ownership to potential competitors or mates. Olfaction is an area of growing interest, but its role in primates, including humans, remains poorly understood. This project will examine olfactory communication in two key species, the ringtailed lemur and mandrill, selected because their exceptional morphological and behavioral characteristics provide an ideal comparative framework for examining olfactory mechanisms of mate choice: Both species have scent glands, but differ dramatically in their social organization and degree of sexual dimorphism. As a nontraditional model, the mandrill also promises to underscore the importance of chemosignals in Old World primates. This project also will survey odorant production in 20 other prosimian species, selected because the diversity of their scent glands and marking behavior offers an equally invaluable opportunity to examine species differences in signal content, with the goal of better understanding phylogenetic patterns. Combined field and laboratory approaches will include (1) chemical analyses to decipher the volatile information content of signals, (2) behavioral observation and bioassays to evaluate the receiver's response to scent signals, (3) genetic analyses to characterize variation in heterozygosity, relatedness, and immunocompatibility between signal senders and their recipients, and (4) proteomic analyses to unravel the nonvolatile contribution to odor cues. This integrative study will identify important correlates of olfactory cues to elucidate the biological mechanisms underlying the evolution of olfactory communication. While focused on primates, the results promise to be broadly applicable, providing additional insight into the role of olfactory signals in mammalian reproductive advertisement, social stratification, and mate choice, as well as in individual, kin, and species recognition. The broader impact of this project will be attained through a strong commitment to teaching and an emphasis on collaboration. This project will (1) provide opportunities for training future scientists; (2) encourage under-represented groups to pursue science careers; (3) foster interdepartmental, inter-university, and international partnerships through new research ventures that broaden the perspectives of faculty and students alike; (4) integrate project-derived information into course development; (5) disseminate information to the scientific community; and (6) share information with educational programs that target universities, primary schools, and the general public, thereby enhancing education, raising public awareness about endangered primates, and aiding in species preservation.

Project Report

Olfactory signals are ubiquitous among mammals and serve to advertise quality, reproductive state, and resource ownership to potential competitors or mates. Olfaction is an area of growing interest, but its role in primates, including humans, remains poorly understood. This project examined olfactory communication in two key species, the ring-tailed lemur and mandrill, selected because their exceptional morphological and behavioral characteristics provide an ideal comparative framework for examining olfactory mechanisms of mate choice: Both species have scent glands, but differ dramatically in their social organization and degree of sex differences. This project also surveyed the scent signals of 20 other prosimian species, selected because the diversity of their scent glands and marking behavior offers an equally invaluable opportunity to examine species differences in signal content, with the goal of better understanding evolutionary patterns. Addressing these questions involved examining animals at two remarkable facilities, the Duke Lemur Center in North Carolina and the Centre International de Recherches M?dicales de Franceville, in Gabon. Access to animals maintained at these facilities, under semi-natural conditions, permitted safe sample collection and behavioral experiments unavailable to field researchers. Using field observations of naturally occurring behavior, we identified potential functions of scent marking in the different species. For instance, if marks are typically deposited around a perimeter, they may function to delineate a territory. Using this approach, we suggested functions relating to the advertisement of sex, dominance status, reproductive state, and possibly identity. We also collected biological samples (blood, DNA, and scent secretions or urine) from the animals to test these putative functions. We used various laboratory techniques to measure hormone concentrations, to obtain genetic fingerprints of the animals, and to decipher the chemical content of their volatile and nonvolatile signals (the portion of the signal that is smelled vs. tasted, respectively). Our hormone analyses revealed differences in reproductive state, whereas our genetic analyses revealed variation in genetic diversity (or ?quality?), and differences in relatedness or compatibility between signal senders and their recipients. We found that the volatile content of signals varied by sex, type of scent, season, reproductive state, dominance status, individual, genetic quality, kinship, species, and evolutionary history (we are still investigating effects of age and health). Some of these same traits were reflected in the nonvolatile fraction. Next, we tested the response of animals to these ?decoded? odors under controlled conditions and found that they responded differently depending on these same variables. For instance, males preferred the scent of breeding vs. nonbreeding females, high-quality vs. low-quality females, intact vs. contracepted females, etc. Together, these different lines of evidence showed that primates can use odor alone to distinguish members of their own species, as well as specific individuals, to recognize unknown relatives, and to identify their ?best? mates or the most worthy opponents. We also showed that different glands convey different kinds of information, and the different olfactory senses (smell and taste) serve to decipher different kinds of information. These signals evolved slowly, but even closely related species have their own olfactory ?signatures.? In female-dominant lemurs, females produce more complex signals than do males; likewise, more socially complex species produce more chemically complex signals. These data suggest that facets of an animal?s social structure are also reflected in scent signals. Analyses specifically comparing lemurs to mandrills are still underway. As a nontraditional model, these latter findings will underscore the importance of chemical signals to the entire Primate Order. While focused on primates, the results are broadly applicable, providing additional insight into the role of olfactory signals in mammalian reproductive advertisement, social stratification, and mate choice, as well as in individual, kin, and species recognition. The broader impact of this project was attained through a strong commitment to teaching and an emphasis on collaboration. This project (1) provided opportunities for training future scientists; (2) encouraged under-represented groups to pursue science careers; (3) fostered interdepartmental, inter-university, and international partnerships through new research ventures that broadened the perspectives of faculty and students alike; (4) integrated project-derived information into course development; (5) disseminated information to the scientific community; and (6) shared information with educational programs that target universities, primary schools, and the general public, thereby enhancing education, raising public awareness about endangered primates, and aiding in species conservation efforts.

Agency
National Science Foundation (NSF)
Institute
Division of Integrative Organismal Systems (IOS)
Application #
0719003
Program Officer
Michelle M. Elekonich
Project Start
Project End
Budget Start
2007-08-01
Budget End
2011-07-31
Support Year
Fiscal Year
2007
Total Cost
$597,869
Indirect Cost
Name
Duke University
Department
Type
DUNS #
City
Durham
State
NC
Country
United States
Zip Code
27705