Mouthing off about developmental stress: Individuality of palate marking in the European badger and its relationship with juvenile parasitoses

Journal of Zoology

Volumn 283, Issue 1, 2011, Pages 52-62

  Nouvellet, P ^a,b   Buesching, C D ^a   Dugdale, H L ^a,c,d   Newman, C ^a   Macdonald, D W ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

^d UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

'animal' model; Coccidia; Developmental instability; European badger; Fitness; Fluctuating asymmetry; Heritability; Individual markings

Indexed keywords

CONSERVATION MANAGEMENT; ENDOPARASITE; ENVIRONMENTAL STRESS; FITNESS; FLUCTUATING ASYMMETRY; HERITABILITY; JUVENILE; LIFE HISTORY TRAIT; MUSTELID; NUMERICAL MODEL; POPULATION STRUCTURE; SPATIAL ANALYSIS; THEORETICAL STUDY; TWO-DIMENSIONAL MODELING;

ANIMALIA; COCCIDIA; MELES MELES;

EID: 78650317041     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/j.1469-7998.2010.00743.x     Document Type: Article

References (77)

1. Anwar, M.A., Newman, C., Macdonald, D.W., Woolhouse, M.E. & Kelly, D.W. (2000). Coccidiosis in the European badger (Meles meles) from England, an epidemiological study. Parasitology 120, 255-260.
2. Apanius, V., Penn, D., Slev, P.R., Ruff, L.R. & Potts, W.K. (1997). The nature of selection on the major histocompatibility complex. Critical Rev. Immunol. 17, 179.
3. Arzoumanian, Z., Holmberg, J. & Norman, B. (2005). An astronomical pattern-matching algorithm for computer-aided identification of whale sharks Rhincodon typus. J. Appl. Ecol. 42, 999.
4. Auger-Methe, M. & Whitehead, H. (2007). The use of natural markings in studies of long-finned pilot whales (Globicephala melas). Mar. Mammal Sci. 23, 77.
5. Brown, T. (1964). Oral pigmentation in the aborigines of Kalumburu, north-west Australia. Arch. Oral Biol. 9, 555.
6. Cheeseman, C.L. & Harris, S. (1982). Methods of marking badgers (Meles meles). J. Zool. (Lond.) 197, 289.
7. Childerhouse, S.J., Dawson, S.M. & Slooten, E. (1996). Stability of fluke marks used in individual photoidentification of male sperm whales at Kaikoura, New Zealand. Mar. Mammal Sci. 12, 447.
8. Clarke, G.M. & McKenzie, L.J. (1992). Fluctuating asymmetry as a quality-control indicator for insect mass rearing processes. J. Econ. Entomol. 85, 2045.
9. Crawley, M.J. (2005). Statistics: An introduction using R. Chichester, UK: Wiley.
10. Crawley, M.J. (2007). The R book. Chichester, UK: Wiley.
11. Donnelly, C.A., Woodroffe, R., Cox, D.R., Bourne, J., Gettinby, G., Le Fevre, A.M., McInerney, J.P. & Morrison, W.I. (2003). Impact of localized badger culling on tuberculosis incidence in British cattle. Nature 426, 834-837.
12. Dufault, S. & Whitehead, H.A.L. (1995). An assessment of changes with time in the marking patterns used for photoidentification of individual sperm whales, Physeter macrocephalus. Mar. Mammal Sci. 11, 335.
13. Dufour, K.W. & Weatherhead, P.J. (1998). Bilateral symmetry and social dominance in captive male red-winged blackbirds. Behav. Ecol. Sociobiol. 42, 71.
14. Dugdale, H.L. (2007). The evolution of social behaviour: the effect of mating system and social structure in the European badger Meles meles. DPhil, University of Oxford, Oxford.
15. Dugdale, H.L., Macdonald, D.W., Pope, L.C. & Burke, T. (2007). Polygynandry, extra-group paternity and multiple-paternity litters in European badger (Meles meles) social groups. Mol. Ecol. 16, 5294-5306.
16. Dugdale, H.L., Nouvellet, P., Pope, L.C., Burke, T. & Macdonald, D.W. (2010). Fitness measures in selection analyses: sensitivity to the overall number of offspring produced in a lifetime. J. Evol. Biol.gy 23, 282-292.
17. Edler, R.J. (2001). Background considerations to facial aesthetics. J. Orthodont. 28, 159.
18. Fagan, W.F. & Holmes, E.E. (2006). Interactive individual identification software (i3s) quantifying the extinction vortex. Ecol. Lett. 9, 51.
19. Falconer, D.S. & Mackay, T.F.C. (1996). Introduction to quantitative genetics, 4th edn. Harlow: Longman.
20. Forcada, J. & Aguilar, A. (2000). Use of photographic identification in capture-recapture studies of mediterranean monk seals. Mar. Mammal Sci. 16, 767.
21. Frankel, J.S. (1991). Inheritance of body marking patterns in the half-banded barb, Barbus-semifasciolatus. J. Hered. 82, 250.
22. Freeman, D.C., Graham, J.H. & Emlen, J.M. (1993). Developmental stability in plants - symmetries, stress and epigenesis. Genetica 89, 97.
23. Gangestad, S.W. & Thornhill, R. (1998). Menstrual cycle variation in women's preferences for the scent of symmetrical men. Proc. Roy. Soc. Lond. Ser. B Biol. Sci. 265, 927.
24. Gangestad, S.W. & Thornhill, R. (1999). Individual differences in developmental precision and fluctuating asymmetry: a model and its implications. J. Evol. Biol. 12, 402.
25. Gilmour, A.R., Gogel, B.J., Cullis, B.R. & Thompson, R. (2006). Asreml user guide release 2.0. Hemel Hempstead: VSN International Ltd.
26. Gope, C., Kehtarnavaz, N., Hillman, G. & Wursig, B. (2005). An affine invariant curve matching method for photo-identification of marine mammals. Pattern Recogn. 38, 125.
27. Gowans, S. & Whitehead, H. (2001). Photographic identification of northern bottlenose whales (Hyperoodon ampullatus): sources of heterogeneity from natural marks. Mar. Mammal Sci. 17, 76.
28. Griffin, J.M., Williams, D.H., Kelly, G.E., Clegg, T.A., O'Boyle, I., Collins, J.D. & More, S.J. (2005). The impact of badger removal on the control of tuberculosis in cattle herds in Ireland. Prev. Vet. Med. 67, 237-266.
29. Guenther, M.M., Ferguson, G.W., Snell, H.L. & Snell, H. (1993). The variation and genetic-basis of dorsal color pattern in the desert side-blotched lizard, Uta-stansburiana-stejnegeri. J. Herpetol. 27, 199.
30. Hadfield, J.D. (2008). Estimating evolutionary parameters when viability selection is operating. Proc. Roy. Soc. Lond. Ser. B Biol. Sci. 275, 723-734.
31. Henderson, C.R. (1976). A simple method for computing the inverse of a numerator relationship matrix used in prediction of breeding values. Biometrics 32, 69.
32. Hereford, J., Hansen, T.F., Houle, D. & Fenster, C. (2004). Comparing strengths of directional selection: how strong is strong? Evolution 58, 2133.
33. Houle, D. (1998). Review: high enthusiasm and low r-squared. Evolution 52, 1872.
34. Johnson, J.B. & Omland, K.S. (2004). Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101.
35. Karanth, K.U. & Nichols, J.D. (1998). Estimation of tiger densities in India using photographic captures and recaptures. Ecology 79, 2852.
36. Karlsson, O., Hiby, L., Lundberg, T., Jussi, M., Jussi, I. & Helander, B. (2005). Photo-identification, site fidelity, and movement of female gray seals (Halichoerus grypus) between haul-outs in the baltic sea. Ambio 34, 628.
37. Kelly, M.J. (2001). Computer-aided photograph matching in studies using individual identification: an example from serengeti cheetahs. J. Mammal. 82, 440.
38. Krebs, J., Anderson, R., Clutton-Brock, T., Morrison, I., Young, D., Donnelly, C., Frost, S. & Woodroffe, R. (1997). Bovine tuberculosis in cattle and badgers PB3423. London: MAFF Publications.
39. Kruuk, H. (1978a). Foraging and spatial-organization of European badger, Meles-meles l. Behav. Ecol. Sociobiol. 4, 75.
40. Kruuk, H. (1978b). Spatial-organization and territorial behavior of European badger Meles meles. J. Zool. 184, 1.
41. Kruuk, L.E.B. (2004). Estimating genetic parameters in natural populations using the 'animal model'. Phil. Trans. Roy. Soc. Lond. Ser. B: Biol. Sci. 359, 873.
42. Lacy, R.C. (1997). Importance of genetic variation to the viability of mammalian populations. J. Mammal. 78, 320.
43. Lande, R. & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution 37, 1210-1226.
44. Leamy, L.J. & Klingenberg, C.P. (2005). The genetics and evolution of fluctuating asymmetry. Annu. Rev. Ecol. Evol. Syst. 36, 1.
45. Lens, L., Dongen, S., Kark, S. & Matthysen, E. (2002). Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol. Rev. 77, 27.
46. Ligon, J.D., Kimball, R. & Merola-Zwartjes, M. (1998). Mate choice by female red junglefowl: the issues of multiple ornaments and fluctuating asymmetry. Anim. Behav. 55, 41.
47. Macdonald, D.W. & Newman, C. (2002). Population dynamics of badgers (Meles meles) in Oxfordshire, UK: numbers, density and cohort life histories, and a possible role of climate change in population growth. J. Zool. (Lond.) 256, 121.
48. Macdonald, D.W., Newman, C., Dean, J., Buesching, C.D. & Johnson, P.J. (2004). The distribution of Eurasian badger, Meles meles, setts in a high-density area: field observations contradict the sett dispersion hypothesis. Oikos 106, 295.
49. Macdonald, D.W., Riordan, P. & Mathews, F. (2006). Biological hurdeles to the control of TB in cattle: a test of two hypotheses concerning wildlife to explain the failure of control. Biol. Conserv. 131, 268-286.
50. Malyon, C. & Healy, S. (1994). Fluctuating asymmetry in antlers of fallow deer, Dama dama, indicates dominance. Anim. Behav. 48, 248.
51. Mateos, C., Alarcos, S., Carranza, J., Sánchez-Prieto, C.B. & Valencia, J. (2008). Fluctuating asymmetry of red deer antlers negatively relates to individual condition and proximity to prime age. Anim. Behav. 75, 1629.
52. Møller, A.P., Cuervo, J.J., Soler, J.J. & Zamora-Muoz, C. (1996). Horn asymmetry and fitness in gemsbok, Oryx g. Gazella. Behav. Ecol. 7, 247.
53. Morris, M.R. (1998). Female preference for trait symmetry in addition to trait size in swordtail fish. Proc. Roy. Soc. Lond. Ser. B Biol. Sci. 265, 907.
54. Newman, C., Macdonald, D.W. & Anwar, M.A. (2001). Coccidiosis in the European badger, Meles meles in Wytham woods: infection and consequences for growth and survival. Parasitology. 123, 133.
55. Nurnberger, B., Barton, N., MacCallum, C., Jason, G. & Appleby, M. (1995). Natural selection on quantitative traits in the bombina hybrid zone. Evolution 49, 1224.
56. Oakes, E.J. & Barnard, P. (1994). Fluctuating asymmetry and mate choice in paradise whydahs, Vidua paradisaea: an experimental manipulation. Anim. Behav. 48, 937.
57. Palmer, A.R. (2000). Quasireplication and the contract of error: lessons from sex ratios, heritabilities and fluctuating asymmetry. Annu. Rev. Ecol. Syst. 31, 441.
58. Pertoldi, C., Back, L.A., Bo Madsen, A., Randi, E. & Loeshcke, V. (2003). Morphological variability and developmental instability in subpopulations of the Eurasian badger (Meles meles) in Denmark. J. Biogeogr. 30, 949-958.
59. Pertoldi, C., Kristensen, T.N.A., Andersen, D.H. & Loeshcke, V. (2006). Developmental instability as an estimator of genetic stress. Heredity 96, 122-127.
60. Pitcairn, R.H. & Hubble-Pitcairn, S. (1989). Natural health for dogs and cats. London: Prion (Multimedia Books Ltd).
61. Polak, M. (1997). Ectoparasitism in mothers causes higher positional fluctuating asymmetry in their sons: implications for sexual selection. Am. Nat. 149, 955.
62. Pope, L.C., Domingo-Roura, X., Erven, K. & Burke, T. (2006). Isolation by distance and gene flow in the Eurasian badger (Meles meles) at both a local and broad scale. Mol. Ecol. 15, 371-386.
63. Roff, D. & Réale, D. (2004). The quantitative genetics of fluctuating asymmetry: a comparison of two models. Evolution 58, 47.
64. Scheib, J.E., Gangestad, S.W. & Thornhill, R. (1999). Facial attractiveness, symmetry and cues of good genes. Proc. Roy. Soc. Lon. Ser. B Biol. Sci. 266, 1913.
65. Sleeman, P., Cussen, R., O'Donoughue, T. & Costello, E. (2001) Badgers (Meles meles) on Fenit island, and their presence or absence on other Islands in co. Kerry, Ireland. Small carnivore conservation, 10.
66. Sokal, R.R. & Rohlf, F.J. (1995). Biometry, 3rd edn. New York: W.H. Freeman & Co.
67. Speed, C., Meekan, M. & Bradshaw, C. (2007). Spot the match - wildlife photo-identification using information theory. Front. Zool. 4, 2.
68. Strobeck, C. (1997). Fluctuating asymmetry and developmental stability: heritability of observable variation vs. heritability of inferred cause. J. Evol. Biol. 10, 39.
69. Thornhill, R. & Gangestad, S.W. (1999a). Facial attractiveness. Trends Cognit. Sci. 3, 452.
70. Thornhill, R. & Gangestad, S.W. (1999b). The scent of symmetry: a human sex pheromone that signals fitness? Evol. Hum. Behav. 20, 175.
71. Thornhill, R. & Møller, A.P. (1997). Developmental stability, disease and medicine. Biol. Rev. 72, 497.
72. Van Dongen, S., Lens, L. & Molenberghs, G. (1999). Mixture analysis of asymmetry: modelling directional asymmetry, antisymmetry and heterogeneity in fluctuating asymmetry. Ecol. Lett. 2, 387.
73. Van Dongen, S.V. (2006). Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. J. Evol. Biol. 19, 1727-1743.
74. Van Tienhoven, A.M., Den Hartog, J.E., Reijns, R.A. & Peddemors, V.M. (2007). A computer-aided program for pattern-matching of natural marks on the spotted raggedtooth shark Carcharias taurus. J. Appl. Ecol. 44, 273.
75. Van Valen, L. (1962). Study of fluctuating asymmetry. Evolution 16, 125.
76. Wilson, A.J., Réale, D., Clements, M.N., Morrissey, M.M., Postma, E., Walling, C.A., Kruuk, L.E.B. & Nussey, D.H. (2010). An ecologist's guide to the animal model. J. Anim. Ecol. 79, 13-26.
77. Woolf, C.M. (1989). Multifactorial inheritance of white facial markings in the Arabian horse. J. Hered. 80, 173.