Naturwissenschaften

, Volume 100, Issue 8, pp 769–777 | Cite as

Relatedness communicated in lemur scent

  • Toni Lyn Morelli
  • R. Andrew Hayes
  • Helen F. Nahrung
  • Thomas E. Goodwin
  • Innocent H. Harelimana
  • Laura J. MacDonald
  • Patricia C. Wright
Original Paper

Abstract

Lemurs are the most olfactory-oriented of primates, yet there is still only a basic level of understanding of what their scent marks communicate. We analyzed scent secretions from Milne-Edwards' sifakas (Propithecus edwardsi) collected in their natural habitat of Ranomafana National Park, Madagascar. We sought to test whether the scent mark could signal genetic relatedness in addition to species, sex, season, and individuality. We not only found correlations (r2 = 0.38, P = 0.017) between the total olfactory fingerprint and genetic relatedness but also between relatedness and specific components of the odor, despite the complex environmental signals from differences in diet and behavior in a natural setting. To the best of our knowledge, this is the first demonstration of an association between genetic relatedness and chemical communication in a wild primate population. Furthermore, we found a variety of compounds that were specific to each sex and each sampling period. This research shows that scent marks could act as a remote signal to avoid inbreeding, optimize mating opportunities, and potentially aid kin selection.

Keywords

Chemical communication Gas chromatography–mass spectrometry (GC–MS) Kin recognition Madagascar Strepsirrhini 

References

  1. Arrigo-Nelson SJ (2006) The impact of habitat disturbance on fruit consumption by the Milne-Edwards' sifaka (Propithecus edwardsi) in Ranomafana National Park, Madagascar. Dissertation, Stony Brook University, Stony BrookGoogle Scholar
  2. Billing AM, Lee AM, Skjelseth S, Borg AA, Hale MC, Slate J, Parn H, Ringsby TH, Saether B-E, Jensen H (2012) Evidence of inbreeding depression but not inbreeding avoidance in a natural house sparrow population. Mol Ecol 21:1487–1499PubMedCrossRefGoogle Scholar
  3. Boulet M, Charpentier MJE, Drea CM (2009) Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate. BMC Evol Biol 9:281PubMedCrossRefGoogle Scholar
  4. Boulet M, Crawford JC, Charpentier MJE, Drea CM (2010) Honest olfactory ornamentation in a female-dominant primate. J Evol Biol 23:1558–1563PubMedCrossRefGoogle Scholar
  5. Burger BV, Viviers MZ, Le Roux NJ, Morris J, Bekker JPI, Le Roux M (2011) Olfactory cue mediated neonatal recognition in sheep, Ovis aries. J Chem Ecol 37:1150–1163PubMedCrossRefGoogle Scholar
  6. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268CrossRefGoogle Scholar
  7. Charpentier MJE, Boulet M, Drea CM (2008) Smelling right: the scent of male lemurs advertises genetic quality and relatedness. Mol Ecol 17:3225–3233PubMedCrossRefGoogle Scholar
  8. Charpentier MJE, Crawford JC, Boulet M, Drea CM (2010) Message ‘scent’: lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues. Anim Behav 80:101–108CrossRefGoogle Scholar
  9. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, PlymouthGoogle Scholar
  10. Dapporto L (2008) The asymmetric scent: ringtailed lemurs (Lemur catta) have distinct chemical signatures in left and right brachial glands. Naturwissenschaften 95:987–991PubMedCrossRefGoogle Scholar
  11. Delbarco-Trillo J, Burkert BA, Goodwin TE, Drea CM (2011) Night and day: the comparative study of strepsirrhine primates reveals socioecological and phylogenetic patterns in olfactory signals. J Evol Biol 24:82–98PubMedCrossRefGoogle Scholar
  12. Dunham AE, Erhart EM, Overdorff DJ, Wright PC (2008) Evaluating effects of deforestation, hunting, and El Nino events on a threatened lemur. Biol Conserv 141:287–297CrossRefGoogle Scholar
  13. Evans CS (1980) Diosmic response to scent-signals in Lemur catta. In: Müller-Schwarze D, Silverstein RM (eds) Chemical signals. Plenum, New York, pp 417–420CrossRefGoogle Scholar
  14. Fisher HS, Swaisgood RR, Fitch-Snyder H (2003) Odor familiarity and female preferences for males in a threatened primate, the pygmy loris Nycticebus pygmaeus: applications for genetic management of small populations. Naturwissenschaften 90:509–512PubMedCrossRefGoogle Scholar
  15. Gallagher M, Wysocki J, Leyden JJ, Spielman AI, Sun X, Preti G (2008) Analyses of volatile organic compounds from human skin. Br J Dermatol 159:780–791PubMedCrossRefGoogle Scholar
  16. Goodwin TE, Brown PA, Eggert MS, Evola MG, House SJ, Morshedi RG, Weddell ME, Chen CJ, Jackson SR, Aubut Y, Eggert J, Schulte BA, Rasmussen LEL (2007) Use of automated solid phase dynamic extraction (SPDE)/GC-MS and novel macros in the search for African elephant pheromones. In: Hurst JL, Beynon RJ, Wyatt TD, Roberts SC (eds) Chemical signals in vertebrates 11. Springer, New York, pp 25–35Google Scholar
  17. Goodwin TE, Broederdorf LJ, Burkert BA, Hirwa HH, Mark DB, Waldrip ZJ, Kopper RA, Sutherland MV, Freeman EW, Hollister-Smith JA, Schulte BA (2012) Chemical signals of elephant musth: temporal aspects of microbially-mediated modifications. J Chem Ecol 38:81–87PubMedCrossRefGoogle Scholar
  18. Gosling LM, Roberts SC (2001) Scent-marking by male mammals: cheat-proof signals to competitors and mates. Adv Stud Behav 30:169–217CrossRefGoogle Scholar
  19. Harrington JE (1977) Discrimination between males and females by scent in Lemur fulvus. Anim Behav 25:147–151PubMedCrossRefGoogle Scholar
  20. Hayes RA, Richardson BJ, Clauus SC, Wylie SG (2002) Semiochemicals and social signaling in the wild European rabbit in Australia: II. Variations in chemical composition of chin gland secretion across sampling sites. J Chem Ecol 28:2613–2625PubMedCrossRefGoogle Scholar
  21. Hayes RA, Morelli TL, Wright PC (2004) Anogenital gland secretions of Lemur catta and Propithecus verreauxi coquereli: a preliminary chemical examination. Am J Primatol 63:49–62PubMedCrossRefGoogle Scholar
  22. Hayes RA, Morelli TL, Wright PC (2006) Volatile components of lemur scent secretions vary throughout the year. Am J Primatol 68:1202–1207PubMedCrossRefGoogle Scholar
  23. Irwin MT, Johnson SE, Wright PC (2005) The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx 39:204–218CrossRefGoogle Scholar
  24. Jemiolo B, Miller KV, Wiesler D, Jelinek I, Novotny M, Marchinton RL (1995) Putative chemical signals from white-tailed deer (Odocoileus virginianus)Urinary and vaginal mucus volatiles excreted by females during breeding season. J Chem Ecol 21:869–879CrossRefGoogle Scholar
  25. Kalinowski ST, Wagner AP, Taper ML (2006) ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molec Ecol Notes 6:576–579CrossRefGoogle Scholar
  26. Kappeler PM (1993) Female dominance in primates and other mammals. In: Bateson PPG, Klopfer PH, Thompson NS (eds) Perspectives in ethology, vol 10, Behaviour and evolution. Plenum, New York, pp 143–158Google Scholar
  27. Karpanty S, Wright PC (2006) Predation on lemurs in the rainforest of Madagascar by multiple predator species: observations and experiments. In: Gursky SL, Nekaris KAI (eds) Primate anti-predator strategies. Springer, New York, pp 75–97Google Scholar
  28. King SJ, Arrigo-Nelson SJ, Pochron ST, Semprebon GM, Godfrey LR, Wright PC, Jernvall J (2005) Dental senescence in a long-lived primate links infant survival to rainfall. Proc Natl Acad Sci USA 102:16579–16583PubMedCrossRefGoogle Scholar
  29. Laska M, Seibt A (2002) Olfactory sensitivity for aliphatic esters in squirrel monkeys and pigtail macaques. Behav Brain Res 134:165–174PubMedCrossRefGoogle Scholar
  30. Lawler RR, Richard AF, Riley MA (2001) Characterization and screening of microsatellite loci in a wild lemur population (Propithecus verreauxi verreauxi). Am J Primatol 55:253–259PubMedCrossRefGoogle Scholar
  31. Leclaire S, Merkling T, Raynaud C, Mulard H, Bessière J-M, Lhuillier E, Hatch SA, Danchin E (2012) Semiochemical compounds of preen secretion reflect genetic make-up in a seabird species. Proc R Soc Lond B 279:1185–1193CrossRefGoogle Scholar
  32. Lipinski J (2001) Automated solid phase dynamic extraction—extraction of organics using a wall coated syringe needle. Fresenius' J Anal Chem 369:57–62CrossRefGoogle Scholar
  33. Martin J, Barja I, Lopez P (2010) Chemical scent constituents in feces of wild Iberian wolves (Canis lupus signatus). Biochem Syst Ecol 38:1096–1102CrossRefGoogle Scholar
  34. Mayor MI, Sommer JA, Huebinger RM, Barber RC, Louis EE (2002) Characterization of seven microsatellite marker loci in a genus of Malagasy lemurs (Propithecus). Mol Ecol Notes 2:385–388CrossRefGoogle Scholar
  35. Morelli TL (2008) Dispersal, kinship, and genetic structure of an endangered Madagascar primate, Propithecus edwardsi. Dissertation, Stony Brook University, Stony BrookGoogle Scholar
  36. Morelli TL, King SJ, Pochron ST, Wright PC (2009) The rules of disengagement: takeovers, infanticide, and dispersal in a rainforest lemur, Propithecus edwardsi. Behavior 146:499–523CrossRefGoogle Scholar
  37. Nahrung HF, Waugh R, Hayes RA (2009) Corymbia species and hybrids: chemical and physical foliar attributes and implications for herbivory. J Chem Ecol 35:1043–1053PubMedCrossRefGoogle Scholar
  38. Osada K, Kashiwayanagi M, Izumi H (2009) Profiles of volatiles in male rat urine: the effect of puberty on the female attraction. Chem Senses 34:713–721PubMedCrossRefGoogle Scholar
  39. Penn DJ, Frommen JG (2010) Kin recognition: an overview of conceptual issues, mechanisms and evolutionary theory. In: Kappeler PM (ed) Animal behaviour: evolution and mechanisms. Springer, Berlin, pp 55–85CrossRefGoogle Scholar
  40. Pochron ST, Tucker WT, Wright PC (2004) Demography, life history, and social structure in Propithecus diadema edwardsi from 1986–2000 in Ranomafana National Park, Madagascar. Am J Phys Anthropol 125:61–72PubMedCrossRefGoogle Scholar
  41. Pochron ST, Morelli TL, Scirbona J, Wright PC (2005a) Sex differences in scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar. Am J Primatol 66:97–110PubMedCrossRefGoogle Scholar
  42. Pochron ST, Morelli TL, Terranova P, Scirbona J, Cohen J, Kunapareddy G, Rakotonirina G, Ratsimbazafy R, Rakotosoa R, Wright PC (2005b) Patterns of male scent-marking in Propithecus edwardsi of Ranomafana National Park, Madagascar. Am J Primatol 65:103–115PubMedCrossRefGoogle Scholar
  43. Price EC, Feistner ATC (1994) Responses of captive aye-ayes (Daubentonia madagascariensis) to the scent of conspecifics—a preliminary investigation. Folia Primatol 62:170–174PubMedCrossRefGoogle Scholar
  44. Rakotoarisoa G, Shore G, McGuire S, Engberg S, Louis E, Brenneman R (2006) Characterization of 20 microsatellite marker loci in Coquerel's sifaka (Propithecus coquereli). Mol Ecol Notes 6:1119–1121CrossRefGoogle Scholar
  45. Ramsay NF, Giller PS (1996) Scent-marking in ring-tailed lemurs: responses to the introduction of “foreign” scent in the home range. Primates 37:13–23CrossRefGoogle Scholar
  46. Ruff JS, Nelson AC, Kubinak JL, Potts WK (2012) MHC signalling during social communication. In: Lopez-Larrea C (ed) Self and nonself (Advances in experimental medicine and biology). Landes Bioscience, Austin, pp 290–313CrossRefGoogle Scholar
  47. Salamon M (1994) Seasonal, sexual and dietary induced variations in the sternal scent secretion in the brushtail possum (Trichosurus vulpecula). In: Apfelbach R, Müller-Schwarze D, Reutier K, Weiber E (eds) Chemical signals in vertebrates VII. Pergamon, Oxford, pp 211–222Google Scholar
  48. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New YorkGoogle Scholar
  49. Schwensow N, Eberle M, Sommer S (2008) Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. Proc R Soc Lond B 275:555–564CrossRefGoogle Scholar
  50. Setchell JM, Vaglio S, Moggi-Cecchi J, Boscaro F, Calamai L, Knapp LA (2010) Chemical composition of scent-gland secretions in an Old World monkey (Mandrillus sphinx): influence of sex, male status, and individual identity. Chem Senses 35:205–220PubMedCrossRefGoogle Scholar
  51. Setchell JM, Vaglio S, Abbott KM, Moggi-Cecchi J, Boscaro F, Pieraccini G, Knapp LA (2011) Odour signals major histocompatibility complex genotype in an Old World monkey. Proc R Soc B 278(1703):274–280PubMedCrossRefGoogle Scholar
  52. Tang-Martinez Z (2001) The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation. Behav Process 53:21–40CrossRefGoogle Scholar
  53. Thom MD, Stockley P, Jury F, Ollier WER, Beynon RJ, Hurst JL (2008) The direct assessment of genetic heterozygosity through scent in the mouse. Curr Biol 18:619–623PubMedCrossRefGoogle Scholar
  54. Thorington KK, Weigl PD (2011) Role of kinship in the formation of southern flying squirrel winter aggregations. J Mammal 92:179–189CrossRefGoogle Scholar
  55. Van Horn RC, Engh AL, Scribner KT, Funk SM, Holekamp KE (2004) Behavioral structuring of relatedness in the spotted hyena (Crocuta crocuta) suggests direct fitness benefits of clan-level cooperation. Mol Ecol 13:449–458PubMedCrossRefGoogle Scholar
  56. Wright PC (1995) Demography and life history of free-ranging Propithecus diadema edwardsi in Ranomafana National Park, Madagascar. Intl J Primatol 16:835–854CrossRefGoogle Scholar
  57. Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yearb Phys Anthropol 42:31–72CrossRefGoogle Scholar
  58. Wright PC, King SJ, Baden A, Jernvall J (2008) Aging in wild female lemurs: sustained fertility with increased infant mortality. Interdis Top Gerontol 36:17–28CrossRefGoogle Scholar
  59. Zabaras R (2003) The evolution of semiochemicals in Australian marsupials. Dissertation, University of Western Sydney, SydneyGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Toni Lyn Morelli
    • 1
    • 6
  • R. Andrew Hayes
    • 2
    • 6
  • Helen F. Nahrung
    • 3
  • Thomas E. Goodwin
    • 4
  • Innocent H. Harelimana
    • 4
  • Laura J. MacDonald
    • 4
  • Patricia C. Wright
    • 5
    • 6
  1. 1.Northeast Climate Science CenterUniversity of MassachusettsAmherstUSA
  2. 2.Department of Agriculture, Fisheries and Forestry, Horticulture and Forestry ScienceAgri-Science QueenslandBrisbaneAustralia
  3. 3.Faculty of Science, Health, Education and EngineeringUniversity of the Sunshine CoastSippy DownsAustralia
  4. 4.Department of ChemistryHendrix CollegeConwayUSA
  5. 5.Department of AnthropologyStony Brook UniversityStony BrookUSA
  6. 6.Centre ValBioRanomafanaMadagascar

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