Mortality trajectory analysis reveals the drivers of sex-specific epidemiology in natural wildlife - Disease interactions

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1790, 2014, Pages

  McDonald, Jennifer L ^a   Smith, Graham C ^b   McDonald, Robbie A ^a   Delahay, Richard J ^b   Hodgson, Dave ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

Badgers; Bayesian; Disease; Sex differences; Survival analysis; Tuberculosis

Indexed keywords

DISEASE SEVERITY; EPIDEMIOLOGY; MORTALITY; MORTALITY RISK; MUSTELID; POPULATION STRUCTURE; SEX-RELATED DIFFERENCE; SURVIVAL; TUBERCULOSIS; WILD POPULATION;

ANIMAL; BAYES THEOREM; BOVINE; EPIDEMIOLOGY; FEMALE; GENETICS; IMMUNOLOGY; LONGITUDINAL STUDY; MALE; MICROBIOLOGY; MORTALITY; MUSTELIDAE; MYCOBACTERIUM BOVIS; SEXUAL DEVELOPMENT; SURVIVAL ANALYSIS; TUBERCULOSIS, BOVINE;

ANIMALS; BAYES THEOREM; CATTLE; EPIDEMIOLOGY; FEMALE; GENETICS; IMMUNOLOGY; LONGITUDINAL STUDIES; MALE; MICROBIOLOGY; MORTALITY; MUSTELIDAE; MYCOBACTERIUM BOVIS; SEX CHARACTERISTICS; SURVIVAL ANALYSIS; TUBERCULOSIS, BOVINE;

EID: 84904704211     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0526     Document Type: Article

References (48)

1. Guerra-Silveira F, Abad-Franch F. 2013 Sex bias in infectious disease epidemiology: patterns and processes. PLoS ONE8, e62390. (doi: 10. 1371/ journal. pone. 0062390)
2. Zuk M, McKean KA. 1996 Sex differences in parasite infections: patterns and processes. Int. J. Parasitol. 26, 1009-1023. (doi: 10. 1016/s0020-7519(96)00086-0)
3. Markle J, Fish E. 2013 SeXX matters in immunity. Trends Immunol. 35, 97-104. (doi: 10. 1016/j. it. 2013. 10. 006)
4. Schuurs A, Verheul HAM. 1990 Effects of gender and sex steroids on the immune-response. J. Steroid Biochem. Mol. Biol. 35, 157-172. (doi: 10. 1016/ 0022-4731(90)90270-3)
5. Bouman A, Heineman MJ, Faas MM. 2005 Sex hormones and the immune response in humans. Hum. Reprod. Update11, 411-423. (doi: 10. 1093/ humupd/dmi008)
6. Klein SL. 2000 The effects of hormones on sex differences in infection: from genes to behavior. Neurosci. Biobehav. Rev. 24, 627-638. (doi: 10. 1016/s0149-7634(00)00027-0)
7. Folstad I, Karter AJ. 1992 Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139, 603-622. (doi: 10. 1086/285346)
8. Zuk M, Stoehr AM. 2002 Immune defense and host life history. Am. Nat. 160, S9-S22. (doi: 10. 1086/342131)
9. Byrnes JP, Miller DC, Schafer WD. 1999 Gender differences in risk taking: a meta-analysis. Psychol. Bull. 125, 367-383. (doi: 10. 1037/0033-2909. 125. 3. 367)
10. Delahay RJ, Walker NJ, Forrester GJ, Harmsen B, Riordan P, MacDonald DW, Newman C, Cheeseman CL. 2006 Demographic correlates of bite wounding in Eurasian badgers, Meles melesL, in stable and perturbed populations. Anim. Behav. 71, 1047-1055. (doi: 10. 1016/j. anbehav. 2005. 07. 018)
11. Macdonald DW, Newman C, Buesching CD, Johnson PJ. 2008 Male-biased movement in a high-density population of the Eurasian badger (Meles meles). J. Mammal. 89, 1077-1086. (doi: 10. 1644/07-mamm-a-185. 1)
12. Colchero F, Clark JS. 2012 Bayesian inference on age-specific survival for censored and truncated data. J. Anim. Ecol. 81, 139-149. (doi: 10. 1111/j. 1365-2656. 2011. 01898. x)
13. Colchero F, Jones OR, Rebke M. 2012 BaSTA: an R package for Bayesian estimation of age-specific mortality from incomplete mark-recapture/recovery data with covariates. Methods Ecol. Evol. 3, 466-470. (doi: 10. 1111/j. 2041-210X. 2012. 00186. x)
14. Graham J, Smith GC, Delahay RJ, Bailey T, McDonald RA, Hodgson D. 2013 Multi-state modelling reveals sex-dependent transmission, progression and severity of tuberculosis in wild badgers. Epidemiol. Infect. 141, 1429-1436. (doi: 10. 1017/ s0950268812003019)
15. Wilkinson D, Smith GC, Delahay RJ, Rogers LM, Cheeseman CL, Clifton-Hadley RS. 2000 The effects of bovine tuberculosis (Mycobacterium bovis)on mortality in a badger (Meles meles) population in England. J. Zool. 250, 389-395. (doi: 10. 1111/j. 1469-7998. 2000. tb00782. x)
16. Donnelly CAet al. 2006 Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature439, 843-846. (doi: 10. 1038/ nature04454)
17. Woolhouse MEJet al. 1997 Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc. Natl Acad. Sci. USA94, 338-342. (doi: 10. 1073/pnas. 94. 1. 338)
18. Delahay RJ, Langton S, Smith GC, Clifton-Hadley RS, Cheeseman CL. 2000 The spatio-temporal distribution ofMycobacterium bovis(bovine tuberculosis) infection in a high-density badger population. J. Anim. Ecol. 69, 428-441. (doi: 10. 1046/j. 1365-2656. 2000. 00406. x)
19. Goodger J, Nolan A, Russell WP, Dalley DJ, Thorns CJ, Stuart FA, Croston P, Newell DG. 1994 Serodiagnosis ofMycobacterium bovisinfection in badgers-development of an indirect ELISA using a 25-kda antigen. Vet. Rec. 135, 82-85. (doi: 10. 1136/vr. 135. 4. 82)
20. Clifton-Hadley RS, Wilesmith JW, Stuart FA. 1993 Mycobacterium bovisin the European badger (Meles meles)-epidemiologic findings in tuberculosis badgers from a naturally infected-population. Epidemiol. Infect. 111, 9-19. (doi: 10. 1017/ S0950268800056624)
21. Gallagher J, Horwill DM. 1977 A selective oleic-acid albumin agar medium for cultivation of Mycobacterium bovis. J. Hyg. 79, 155-160. (doi: 10. 1017/S0022172400052943)
22. Vicente J, Delahay RJ, Walker NJ, Cheeseman CL. 2007 Social organization and movement influence the incidence of bovine tuberculosis in an undisturbed high-density badgerMeles meles population. J. Anim. Ecol. 76, 348-360. (doi: 10. 1111/j. 1365-2656. 2006. 01199. x)
23. Greenwald Ret al. 2003 Improved serodetection of Mycobacterium bovisinfection in badgers (Meles meles) using multiantigen test formats. Diagn. Microbiol. Infect. Dis. 46, 197-203. (doi: 10. 1016/ s0732-8893(03)00046-4)
24. Clifton-Hadley RS, Sayers AR, Stock MP. 1995 Evaluation of an ELISA forMycobacterium bovis infection in badgers (Meles meles). Vet. Rec. 137, 555-558. (doi: 10. 1136/vr. 137. 22. 555)
25. Drewe JA, Tomlinson AJ, Walker NJ, Delahay RJ. 2010 Diagnostic accuracy and optimal use of three tests for tuberculosis in live badgers. PLoS ONE5, e11196. (doi: 10. 1371/journal. pone. 0011196)
26. R Development Core Team. 2013R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
27. McDonald DB, Fitzpatrick JW, Woolfenden GE. 1996 Actuarial senescence and demographic heterogeneity in the Florida Scrub Jay. Ecology77, 2373-2381. (doi: 10. 2307/2265739)
28. Vaupel JW, Manton KG, Stallard E. 1979 Impact of heterogeneity in individual frailty on the dynamics of mortality. Demography16, 439-454. (doi: 10. 2307/2061224)
29. Spiegelhalter DJ, Best NG, Carlin BP, Van Der Linde A. 2002 Bayesian measures of model complexity and fit. J. R. Stat. Soc. B 64, 583-639. (doi: 10. 1111/1467-9868. 00353)
30. Kullback S, Leibler RA. 1951 On information and sufficiency. Ann. Math. Stat. 22, 79-86. (doi: 10. 1214/aoms/1177729694)
31. Celeux G, Forbes F, Robert CP, Titterington DM. 2006 Deviance information criteria for missing data models. Bayesian Anal. 1, 651-673. (doi: 10. 1214/ 06-BA122)
32. Clutton-Brock TH, Isvaran K. 2007 Sex differences in ageing in natural populations of vertebrates. Proc. R. Soc. B274, 3097-3104. (doi: 10. 1098/rspb. 2007. 1138)
33. Tomlinson AJ, Chambers MA, Wilson GJ, McDonald RA, Delahay RJ. 2013 Sex-related heterogeneity in the life-history correlates of Mycobacterium bovis infection in European badgers (Meles meles). Transboundary Emerg. Dis. 60, 37-45. (doi: 10. 1111/tbed. 12097)
34. Lochmiller RL, Deerenberg C. 2000 Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos88, 87-98. (doi: 10. 1034/j. 1600-0706. 2000. 880110. x)
35. Sheldon BC, Verhulst S. 1996 Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321. (doi: 10. 1016/0169-5347(96)10039-2)
36. Prall SP, Muehlenbein MP. 2013 Testosterone and immune function in primates: a brief summary with methodological considerations. Int. J. Primatol. 59, 1-20. (doi: 10. 1007/s10764-014-9752-x)
37. Mills SC, Grapputo A, Jokinen I, Koskela E, Mappes T, Poikonen T. 2010 Fitness trade-offs mediated by immunosuppression costs in a small mammal. Evolution64, 166-179. (doi: 10. 1111/j. 1558-5646. 2009. 00820. x)
38. Moore SL, Wilson K. 2002 Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015-2018. (doi: 10. 1126/ science. 1074196)
39. Verhulst S, Dieleman SJ, Parmentier HK. 1999 A tradeoff between immunocompetence and sexual ornamentation in domestic fowl. Proc. Natl Acad. Sci. USA96, 4478-4481. (doi: 10. 1073/pnas. 96. 8. 4478)
40. Saino N, Galeotti P, Sacchi R, Moller AP. 1997 Song and immunological condition in male barn swallows (Hirundo rustica). Behav. Ecol. 8, 364-371. (doi: 10. 1093/beheco/8. 4. 364)
41. Svensson E, Sinervo B, Comendant T. 2001 Densitydependent competition and selection on immune function in genetic lizard morphs. Proc. Natl Acad. Sci. USA98, 12 561-12 565. (doi: 10. 1073/pnas. 211071298)
42. Cavigelli SA, Pereira ME. 2000 Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm. Behav. 37, 246-255. (doi: 10. 1006/hbeh. 2000. 1585)
43. Rogers LM, Cheeseman CL, Mallinson PJ, CliftonHadley R. 1997 The demography of a highdensity badger (Meles meles) population in the west of England. J. Zool. 242, 705-728. (doi: 10. 1111/j. 1469-7998. 1997. tb05821. x)
44. Klein SL. 2003 Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol. Behav. 79, 441-449. (doi: 10. 1016/s0031-9384(03)00163-x)
45. Vyas A, Kim S-K, Giacomini N, Boothroyd JC, Sapolsky RM. 2007 Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc. Natl Acad. Sci. USA 104, 6442-6447. (doi: 10. 1073/pnas. 0608310104)
46. Jenkins HE, Cox DR, Delahay RJ. 2012 Direction of association between bite wounds and Mycobacterium bovisinfection in badgers: implications for transmission. PLoS ONE7, e45584. (doi: 10. 1371/journal. pone. 0045584)
47. Woodroffe Ret al. 2006 Culling and cattle controls influence tuberculosis risk for badgers. Proc. Natl Acad. Sci. USA103, 14 713-14 717. (doi: 10. 1073/ pnas. 0606251103)
48. Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P. 2006 Seasonality and the dynamics of infectious diseases. Ecol. Lett. 9, 467-484. (doi: 10. 1111/j. 1461-0248. 2005. 00879. x)