Symbiotic bacteria appear to mediate hyena social odors

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 49, 2013, Pages 19832-19837

  Theis, Kevin R ^a,b   Venkataraman, Arvind ^a   Dycus, Jacquelyn A ^a   Koonter, Keith D ^a   Schmitt Matzen, Emily N ^a   Wagner, Aaron P ^b   Holekamp, Kay E ^b,c   Schmidt, Thomas M ^a,b  

^a Departments of Microbiology and Molecular Genetics   (United States)

^b Zoology ^*  (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VOLATILE FATTY ACID;

ANIMAL BEHAVIOR; ANIMAL COMMUNICATION; ARTICLE; BODILY SECRETIONS; FERMENTATION; HYENA; MICROBIAL COMMUNITY; MICROBIOME; NONHUMAN; ODOR; PRIORITY JOURNAL; SCENT GLAND; SYMBIOSIS;

ANIMAL BEHAVIOR; ANIMAL COMMUNICATION; MICROBIOME;

ANIMAL COMMUNICATION; ANIMALS; BACTERIA; BASE SEQUENCE; DNA PRIMERS; FATTY ACIDS, VOLATILE; FEMALE; FERMENTATION; HYAENIDAE; KENYA; MALE; MICROBIOTA; MOLECULAR SEQUENCE DATA; ODORS; RNA, RIBOSOMAL, 16S; SCENT GLANDS; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 84889684986     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1306477110     Document Type: Article

References (51)

1. Gilbert SF, Sapp J, Tauber AI (2012) A symbiotic view of life: We have never been individuals. Q Rev Biol 87(4):325-341.
2. McFall-Ngai M, et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110(9):3229-3236.
3. Fraune S, Bosch TCG (2010) Why bacteria matter in animal development and evolution. Bioessays 32(7):571-580.
4. Forsythe P, Kunze WA, Bienenstock J (2012) On communication between gut microbes and the brain. Curr Opin Gastroenterol 28(6):557-562.
5. Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336(6086):1268-1273.
6. Archie EA, Theis KR (2011) Animal behaviour meets microbial ecology. Anim Behav 82(3):425-436.
7. Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB (2012) Microbiology. Animal behavior and the microbiome. Science 338(6104):198-199.
8. Wyatt TD (2010) Pheromones and signature mixtures: Defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196(10):685-700.
9. Steiger S, Schmitt T, & Schaefer HM (2011) The origin and dynamic evolution of chemical information transfer. Proc Biol Sci 278(1708):970-979.
10. Albone ES (1984) Mammalian Semiochemistry (John Wiley, New York).
11. Gorman ML, Nedwell DB, Smith RM (1974) An analysis of the contents of the anal scent pockets of Herpestes auropunctatus (Carnivora: Viverridae). J Zool 172:389-399.
12. Albone ES, Eglinton G, Walker JM, Ware GC (1974) The anal sac secretion of the red fox (Vulpes vulpes); its chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo). Life Sci 14(2):387-400.
13. Blackwood CB, Hudleston D, Zak DR, Buyer JS (2007) Interpreting ecological diversity indices applied to terminal restriction fragment length polymorphism data: Insights from simulated microbial communities. Appl Environ Microbiol 73(16):5276-5283.
14. Sin YW, Buesching CD, Burke T, Macdonald DW (2012) Molecular characterization of the microbial communities in the subcaudal gland secretion of the European badger (Meles meles). FEMS Microbiol Ecol 81(3):648-659.
15. Theis KR, Schmidt TM, & Holekamp KE (2012) Evidence for a bacterial mechanism for group-specific social odors among hyenas. Sci. Rep. 2.
16. Burgener N, East ML, Hofer H, DehnhardM (2008) Do spotted hyena scent marks code for clan membership? Chemical Signals in Vertebrates 11, eds Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (Springer, New York), pp 169-178.
17. Holekamp KE, Dloniak SM (2010) Intraspecific variation in the behavioral ecology of a tropical carnivore, the spotted hyena. Adv Stud Behav 42:189-229.
18. Boydston EE, Morelli TL, Holekamp KE (2001) Sex differences in territorial behavior exhibited by the spotted hyena (Hyaenidae, Crocuta crocuta). Ethology 107(5): 369-385.
19. Kruuk H (1972) The Spotted Hyena: A Study of Predation and Social Behavior (Univ of Chicago Press, Chicago).
20. Mills MGL (1990) Kalahari Hyenas: Comparative Behavioral Ecology of Two Species (Chapman & Hall, New York).
21. Wagner AP, Frank LG, Creel S (2008) Spatial grouping in behaviourally solitary striped hyaenas, Hyaena hyaena. Anim Behav 75(3):1131-1142.
22. Holekamp KE, Kolowski JM (2009) Hyaenidae. Handbook of Mammals of the World, eds Wilson D, Mittermeier R, Fonseca G (Lynx Edicions, Madrid), pp 234-260.
23. Buglass AJ, Darling FMC, Waterhouse JS (1990) Analysis of the anal sac secretion of the Hyaenidae. Chemical Signals in Vertebrates 5, eds Macdonald DW, Muller-Schwarze D, Natynczuk SE (Kluwer Academic/Plenum Publishers, New York), pp 65-69.
24. Burgener N, Dehnhard M, Hofer H, East ML (2009) Does anal gland scent signal identity in the spotted hyaena? Anim Behav 77(3):707-715.
25. Drea CM, Vignieri SN, Kim HS, Weldele ML, Glickman SE (2002) Responses to olfactory stimuli in spotted hyenas (Crocuta crocuta): II. Discrimination of conspecific scent. J Comp Psychol 116(4):342-349.
26. Sheneman L, Evans J, Foster JA (2006) Clearcut: A fast implementation of relaxed neighbor joining. Bioinformatics 22(22):2823-2824.
27. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261-5267.
28. Schleifer K-H (2009) Phylum 13. Firmicutes Gibbons and Murray 1978, 5. Bergey's Manual of Systematic Bacteriology, eds Vos P, et al. (Springer, New York), pp 19-1317.
29. Ezaki T, Li N, Kawamura Y (2006) The anaerobic gram-positive cocci. Prokaryotes 4:795-808.
30. Stackebrandt E, Cummins CS, Johnson JL (2006) Family Propionibacteriaceae: The Genus Propionibacterium. Prokaryotes 3:400-418.
31. Bernard KA, Munro C, Wiebe D, Ongsansoy E (2002) Characteristics of rare or recently described corynebacterium species recovered from human clinical material in Canada. J Clin Microbiol 40(11):4375-4381.
32. Hofstad T (2006) The genus Fusobacterium. Prokaryotes 7:1016-1027.
33. Gibson FC, Genco CA (2006) The genus Porphyromonas. Prokaryotes 7:428-454.
34. Xu Y, et al. (2007) Comparison of human axillary odour profiles obtained by gas chromatography/mass spectrometry and skin microbial profiles obtained by denaturing gradient gel electrophoresis using multivariate pattern recognition. Metabolomics 3(4):427-437.
35. Zomer S, et al. (2009) Consensus multivariate methods in gas chromatography mass spectrometry and denaturing gradient gel electrophoresis: MHC-congenic and other strains of mice can be classified according to the profiles of volatiles and microflora in their scent-marks. Analyst (Lond) 134(1):114-123.
36. Hofer H, Mills G (1998) Worldwide distribution of hyaenas. Hyaenas: Status Survey and Conservation Action Plan, eds Mills G, Hofer H (International Union for the Conservation of Nature, Cambridge, UK), pp 40-63.
37. Ord TJ, King L, Young AR (2011) Contrasting theory with the empirical data of species recognition. Evolution 65(9):2572-2591.
38. Freeberg TM, Dunbar RIM, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Philos Trans R Soc Lond B Biol Sci 367(1597):1785-1801.
39. delBarco-Trillo J, Sacha CR, Dubay GR, Drea CM (2012) Eulemur, me lemur: The evolution of scent-signal complexity in a primate clade. Philos Trans R Soc Lond B Biol Sci 367(1597):1909-1922.
40. Theis KR, Heckla AL, Verge JR, Holekamp KE (2008) The ontogeny of pasting behavior in free-living spotted hyenas, Crocuta crocuta. Chemical Signals in Vertebrates 11, eds Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (Springer, New York), pp 179-188.
41. Koren O, et al. (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150(3):470-480.
42. Hickey RJ, Zhou X, Pierson JD, Ravel J, Forney LJ (2012) Understanding vaginal microbiome complexity from an ecological perspective. Transl Res 160(4):267-282.
43. Armitage GC (2013) Bi-directional relationship between pregnancy and periodontal disease. Periodontol 2000 61(1):160-176.
44. Dloniak SM, et al. (2004) Non-invasive monitoring of fecal androgens in spotted hyenas (Crocuta crocuta). Gen Comp Endocrinol 135(1):51-61.
45. Van Meter PE, et al. (2008) Non-invasive measurement of fecal estrogens in the spotted hyena (Crocuta crocuta). Gen Comp Endocrinol 155(2):464-471.
46. Barzantny H, Brune I, Tauch A (2012) Molecular basis of human body odour formation: Insights deduced from corynebacterial genome sequences. Int J Cosmet Sci 34(1):2-11.
47. Thornton MJ (2002) The biological actions of estrogens on skin. Exp Dermatol 11(6): 487-502.
48. Zouboulis CC, Chen WC, Thornton MJ, Qin K, Rosenfield R (2007) Sexual hormones in human skin. Horm Metab Res 39(2):85-95.
49. Schloss PD, et al. (2009) Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537-7541.
50. Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62(2):142-160.
51. McCune B, Grace JB (2002) Analysis of Ecological Communities (MjM Software Design, Gleneden Beach, OR).