Bacteria and the evolution of honest signals. The case of ornamental throat feathers in spotless starlings

Functional Ecology

Volumn 29, Issue 5, 2015, Pages 701-709

  Ruiz Rodríguez, Magdalena ^a   Tomás, Gustavo ^a   Martín Gálvez, David ^a,b   Ruiz Castellano, Cristina ^a   Soler, Juan José ^a  

^a DEPARTAMENTO DE ECOLOGÍA FUNCIONAL Y EVOLUTIVA   (Spain)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Sturnus unicolor; Bacterial load; Feather degrading bacteria; Ornaments; Sexual selection; Uropygial gland

Indexed keywords

DEGRADATION; ENVIRONMENTAL RESPONSE; FEATHER; GROWTH RESPONSE; MICROBIAL ACTIVITY; ORNAMENTAL SPECIES; SECRETION; SEX-RELATED DIFFERENCE; SIGNALING;

ANIMALIA; BACTERIA (MICROORGANISMS); STURNIDAE; STURNUS UNICOLOR;

EID: 84929518917     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12376     Document Type: Article

References (55)

1. Amo, L., Avilés, J.M., Parejo, D., Peña, A., Rodríguez, J. & Tomás, G. (2012) Sex recognition by odour and variation in the uropygial gland secretion in starlings. Journal of Animal Ecology, 81, 605-613.
2. Aparicio, J.M., Cordero, P.J. & Veiga, J.P. (2001) A test of the hypothesis of mate choice based on heterozygosity in the spotless starling. Animal Behaviour, 62, 1001-1006.
3. Bonser, R.H.C. (1995) Melanin and the abrasion resistance of feathers. The Condor, 97, 590-591.
4. Burtt, E.H. (1986) An analysis of physical, physiological, and optical aspects of avian coloration with emphasis on wood-warblers. Ornithological Monographs, 38, 1-126.
5. Burtt, E.H. & Ichida, J.M. (1999) Occurrence of feather-degrading bacilli in the plumage of birds. The Auk, 116, 364-372.
6. Burtt, E.H. & Ichida, J.M. (2004) Gloger's rule, feather-degrading bacteria, and color variation among Song Sparrows. The Condor, 106, 681-686.
7. Burtt, E.H., Schroeder, M.R., Smith, L.A., Sroka, J.E. & Mcgraw, K.J. (2011) Colourful parrot feathers resist bacterial degradation. Biology Letters, 7, 214-216.
8. Clayton, D.H. (1991) The influence of parasites on host sexual selection. Parasitology Today, 7, 329-334.
9. Cramp (1998) The Complete List of the Western Palearctic. BWP on CD Rom. Oxford University Press, Oxford.
10. Czirjak, G.A., Pap, P.L., Vagasi, C.I., Giraudeau, M., Muresan, C., Mirleau, P. et al. (2013) Preen gland removal increases plumage bacterial load but not that of feather-degrading bacteria. Naturwissenschaften, 100, 145-151.
11. Endler, J.A. (1993) Some general comments on the evolution and design of animal communication systems. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 340, 215-225.
12. Folstad, I. & Karter, A.J. (1992) Parasites, bright males, and the immunocompetence handicap. American Naturalist, 139, 603-622.
13. Gil, D. & Culver, R. (2011) Male ornament size in a passerine predicts the inhibitory effect of testosterone on macrophage phagocytosis. Functional Ecology, 25, 1278-1283.
14. Giraudeau, M., Czirjak, G.A., Duval, C., Bretagnolle, V., Gutierrez, C., Guillon, N. et al. (2013) Effect of preen oil on plumage bacteria: an experimental test with the mallard. Behavioural Processes, 92, 1-5.
15. Goldstein, G., Flory, K.R., Browne, B.A., Majid, S., Ichida, J.M. & Burtt, E.H. (2004) Bacterial degradation of black and white feathers. The Auk, 121, 656-659.
16. Gunderson, A.R., Forsyth, M.H. & Swaddle, J.P. (2009) Evidence that plumage bacteria influence feather coloration and body condition of eastern bluebirds Sialia sialis. Journal of Avian Biology, 40, 440-447.
17. Gunderson, A.R., Frame, A.M., Swaddle, J.P. & Forsyth, M.H. (2008) Resistance of melanized feathers to bacterial degradation: is it really so black and white? Journal of Avian Biology, 39, 539-545.
18. Hamilton, W.D. & Zuk, M. (1982) Heritable true fitness and bright birds - A role for parasites. Science, 218, 384-387.
19. Horrocks, N.P.C., Matson, K.D., Shobrak, M., Tinbergen, J.M. & Tieleman, B.I. (2012) Seasonal patterns in immune indices reflect microbial loads on birds but not microbes in the wider environment. Ecosphere, 3, 19.
20. Jacob, S., Immer, A., Leclaire, S., Parthuisot, N., Ducamp, C., Espinasse, G. et al. (2014) Uropygial gland size and composition varies according to experimentally modified microbiome in Great tits. BMC Evolutionary Biology, 14, 134.
21. Lezana, L., Miranda, R., Campos, F. & Peris, S.J. (2000) Sex differentiation in the spotless starling (Sturnus unicolor, Temminck 1820). Belgian Journal of Zoology, 130, 139-142.
22. López-Rull, I., Celis, P. & Gil, D. (2007) Egg colour covaries with female expression of a male ornament in the spotless starling (Sturnus unicolor). Ethology, 113, 926-933.
23. Martín-Platero, A.M., Valdivia, E., Ruiz-Rodríguez, M., Soler, J.J., Martín-Vivaldi, M., Maqueda, M. et al. (2006) Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10-3, isolated from the uropygial gland of the hoopoe (Upupa epops). Applied and Environmental Microbiology, 72, 4245-4249.
24. Martín-Vivaldi, M., Ruiz-Rodríguez, M., Soler, J.J., Peralta-Sánchez, J.M., Mendez, M., Valdivia, E. et al. (2009) Seasonal, sexual and developmental differences in hoopoe Upupa epops preen gland morphology and secretions: evidence for a role of bacteria. Journal of Avian Biology, 40, 191-205.
25. Martín-Vivaldi, M., Peña, A., Peralta-Sánchez, J.M., Sánchez, L., Ananou, S., Ruiz-Rodríguez, M. et al. (2010) Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proceedings of the Royal Society B-Biological Sciences, 277, 123-130.
26. Maynard-Smith, J. & Harper, D. (2003) Animal Signals. Oxford Series in Ecology and Evolution. Oxford University Press, Oxford.
27. McFall-Ngai, M., Hadfield, M.G., Bosch, T.C.G., Carey, H.V., Domazet-Lošo, T., Douglas, A.E. et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, 110, 3229-3236.
28. Møller, A.P., Christe, P. & Lux, E. (1999) Parasitism, host immune function, and sexual selection. The Quarterly Review of Biology, 74, 3-20.
29. Møller, A.P., Czirjak, G.A. & Heeb, P. (2009) Feather micro-organisms and uropygial antimicrobial defences in a colonial passerine bird. Functional Ecology, 23, 1097-1102.
30. Navarro, C., Perez-Contreras, T., Aviles, J.M., Mcgraw, K.J. & Soler, J.J. (2010) Beak colour reflects circulating carotenoid and vitamin A levels in spotless starlings (Sturnus unicolor). Behavioral Ecology and Sociobiology, 64, 1057-1067.
31. Pap, P.L., Vagasi, C.I., Barbos, L. & Marton, A. (2013) Chronic coccidian infestation compromises flight feather quality in house sparrows Passer domesticus. Biological Journal of the Linnean Society, 108, 414-428.
32. Peele, A.M., Burtt, E.H., Schroeder, M.R. & Greenberg, R.S. (2009) Dark color of the coastal plain Swamp Sparrow (Melospiza georgiana nigrescens) may be an evolutionary response to occurrence and abundance of salt-tolerant feather-degrading Bacilli in its plumage. The Auk, 126, 531-535.
33. Piault, R., Gasparini, J., Bize, P., Paulet, M., Mcgraw, K.J. & Roulin, A. (2008) Experimental support for the makeup hypothesis in nestling tawny owls (Strix aluco). Behavioral Ecology, 19, 703-709.
34. Playfair, J. & Bancroft, G. (2004) Infection and Immunity. Oxford University Press, Oxford.
35. Poulin, R. (1998) Evolutionary Ecology of Parasites. Chapman & Hall, London.
36. Proctor, H.C. (2003) Feather mites (Acari: Astigmata): ecology, behavior, and evolution. Annual Review of Entomology, 48, 185-209.
37. Ruiz de Castañeda, R., Burtt, E.H., Gonzalez-Braojos, S. & Moreno, J. (2012) Bacterial degradability of an intrafeather unmelanized ornament: a role for feather-degrading bacteria in sexual selection? Biological Journal of the Linnean Society, 105, 409-419.
38. Ruiz-Rodriguez, M., Tomás, G., Martín-Gálvez, D., Ruiz-Castellano, C. & Soler, J. (2014) Data from: Bacteria and the evolution of honest signals. The case of ornamental throat feathers in spotless starlings. Dryad Digital Repository. http://dx.doi.org/10.5061/dryad.p69n4.
39. Ruiz-Rodríguez, M., Valdivia, E., Soler, J.J., Martín-Vivaldi, M., Martín-Platero, A.M. & Martínez-Bueno, M. (2009) Symbiotic bacteria living in the hoopoe's uropygial gland prevent feather degradation. Journal of Experimental Biology, 212, 3621-3626.
40. Ruiz-Rodríguez, M., Martínez-Bueno, M., Martín-Vivaldi, M., Valdivia, E. & Soler, J.J. (2013) Bacteriocins with a broader antimicrobial spectrum prevail in enterococcal symbionts isolated from the hoopoe's uropygial gland. FEMS Microbiology Ecology, 85, 495-502.
41. Ruxton, G.D. & Schaefer, H.M. (2011) Resolving current disagreements and ambiguities in the terminology of animal communication. Journal of Evolutionary Biology, 24, 2574-2585.
42. Senar, J.C. (1999) La medición de la repetibilidad y el error de medida. Etologuia, 17, 53-64.
43. Shawkey, M.D., Pillai, S.R. & Hill, G.E. (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. Journal of Avian Biology, 34, 345-349.
44. Shawkey, M.D., Pillai, S.R. & Hill, G.E. (2009) Do feather-degrading bacteria affect sexually selected plumage color? Naturwissenschaften, 96, 123-128.
45. Shawkey, M.D., Mills, K.L., Dale, C. & Hill, G.E. (2005) Microbial diversity of wild bird feathers revealed through culture-based and culture-independent techniques. Microbial Ecology, 50, 40-47.
46. Shawkey, M.D., Pillai, S.R., Hill, G.E., Siefferman, L.M. & Roberts, S.R. (2007) Bacteria as an agent for change in structural plumage color: correlational and experimental evidence. American Naturalist, 169, S112-S121.
47. Soler, J.J., Navarro, C., Contreras, T., Avilés, J.M. & Cuervo, J.J. (2008) Sexually selected egg coloration in spotless starlings. American Naturalist, 171, 183-194.
48. Soler, J.J., Peralta Sánchez, J.M., Flensted-Jensen, E., Martín Platero, A.M. & Møller, A.P. (2011) Innate humoral immunity reduces eggshell bacterial load of European birds: a comparative analysis. Naturwissenschaften, 98, 807-813.
49. Soler, J.J., Peralta-Sánchez, J.M., Martín-Platero, A.M., Martín-Vivaldi, M., Martínez-Bueno, M. & Møller, A.P. (2012) The evolution of size of the uropygial gland: mutualistic feather mites and uropygial secretion reduce bacterial loads of eggshells and hatching failures of European birds. Journal of Evolutionary Biology, 25, 1779-1791.
50. Statsoft, Inc. 2005. STATISTICA (data analysis software system), version 7.1. www.statsoft.com.
51. Vincze, O., Vagasi, C.I., Kovacs, I., Galvan, I. & Pap, P.L. (2013) Sources of variation in uropygial gland size in European birds. Biological Journal of the Linnean Society, 110, 543-563.
52. Westneat, D.F. (2012) Evolution in response to social selection: the importance of interactive effects of traits on fitness. Evolution, 66, 890-895.
53. Zirpoli, J.A., Black, J.M. & Gabriel, P.O. (2013) Parasites and plumage in Steller's jays: an experimental field test of the parasite-mediated handicap hypothesis. Ethology Ecology & Evolution, 25, 103-116.
54. Zuk, M. (1992) The role of parasites in sexual selection - Current evidence and future-directions. Advances in the Study of Behavior, 21, 39-68.
55. Zuk, M. & Johnsen, T.S. (2000) Social environment and immunity in male red jungle fowl. Behavioral Ecology, 11, 146-153.