Timing and severity of immunizing diseases in rabbits is controlled by seasonal matching of host and pathogen dynamics

Infectious diseases can exert a strong influence on the dynamics of host populations, but it remains unclear why such disease-mediated control only occurs under particular environmental conditions. We used 16 years of detailed field data on invasive European rabbits (Oryctolagus cuniculus) in Australia, linked to individual-based stochastic models and Bayesian approximations, to test whether (i) mortality associated with rabbit haemorrhagic disease (RHD) is driven primarily by seasonal matches/mismatches between demographic rates and epidemiological dynamics and (ii) delayed infection (arising from insusceptibility and maternal antibodies in juveniles) are important factors in determining disease severity and local population persistence of rabbits. We found that both the timing of reproduction and exposure to viruses drove recurrent seasonal epidemics of RHD. Protection conferred by insusceptibility and maternal antibodies controlled seasonal disease outbreaks by delaying infection; this could have also allowed escape from disease. The persistence of local populations was a stochastic outcome of recovery rates from both RHD and myxomatosis. If susceptibility to RHD is delayed, myxomatosis will have a pronounced effect on population extirpation when the two viruses coexist. This has important implications for wildlife management, because it is likely that such seasonal interplay and disease dynamics has a strong effect on long-term population viability for many species.

[1]  S. Sommer,et al.  Rabbit haemorrhagic disease: virus persistence and adaptation in Australia , 2014, Evolutionary applications.

[2]  R. Plowright,et al.  The effect of seasonal birth pulses on pathogen persistence in wild mammal populations , 2014, Proceedings of the Royal Society B: Biological Sciences.

[3]  Damien A. Fordham,et al.  Effects of prey metapopulation structure on the viability of black-footed ferrets in plague-impacted landscapes: a metamodelling approach , 2014 .

[4]  D. Peacock,et al.  Is increased juvenile infection the key to recovery of wild rabbit populations from the impact of rabbit haemorrhagic disease? , 2014, European Journal of Wildlife Research.

[5]  D. Pontier,et al.  Early infections by myxoma virus of young rabbits (Oryctolagus cuniculus) protected by maternal antibodies activate their immune system and enhance herd immunity in wild populations , 2014, Veterinary Research.

[6]  Damien A. Fordham,et al.  Life history and spatial traits predict extinction risk due to climate change , 2014 .

[7]  E. Holmes,et al.  Molecular epidemiology of Rabbit Haemorrhagic Disease Virus in Australia: when one became many , 2014, Molecular ecology.

[8]  Robert C. Lacy,et al.  Metamodels for Transdisciplinary Analysis of Wildlife Population Dynamics , 2013, PloS one.

[9]  B. Grenfell,et al.  Impact of Birth Seasonality on Dynamics of Acute Immunizing Infections in Sub-Saharan Africa , 2013, PloS one.

[10]  E. Holmes,et al.  Genome Scale Evolution of Myxoma Virus Reveals Host-Pathogen Adaptation and Rapid Geographic Spread , 2013, Journal of Virology.

[11]  John D. Wright,et al.  The non-pathogenic Australian rabbit calicivirus RCV-A1 provides temporal and partial cross protection to lethal Rabbit Haemorrhagic Disease Virus infection which is not dependent on antibody titres , 2013, Veterinary Research.

[12]  Bernt-Erik Sæther,et al.  Population Growth in a Wild Bird Is Buffered Against Phenological Mismatch , 2013, Science.

[13]  G. Saunders,et al.  The Economic Benefits of the Biological Control of Rabbits in A ustralia, 1950–2011 , 2013 .

[14]  Christopher N. Johnson,et al.  No need for disease: testing extinction hypotheses for the thylacine using multi-species metamodels. , 2013, The Journal of animal ecology.

[15]  Damien A. Fordham,et al.  European rabbit survival and recruitment are linked to epidemiological and environmental conditions in their exotic range. , 2012 .

[16]  P. Kerr Myxomatosis in Australia and Europe: a model for emerging infectious diseases. , 2012, Antiviral research.

[17]  P. Klepac,et al.  Impact of birth rate, seasonality and transmission rate on minimum levels of coverage needed for rubella vaccination , 2012, Epidemiology and Infection.

[18]  J. Le Pendu,et al.  Rabbit haemorrhagic disease (RHD) and rabbit haemorrhagic disease virus (RHDV): a review , 2012, Veterinary Research.

[19]  Damien A. Fordham,et al.  Novel coupling of individual-based epidemiological and demographic models predicts realistic dynamics of tuberculosis in alien buffalo , 2012 .

[20]  A. Gelman,et al.  Multiple Imputation with Diagnostics (mi) in R: Opening Windows into the Black Box , 2011 .

[21]  Christian P Robert,et al.  Lack of confidence in approximate Bayesian computation model choice , 2011, Proceedings of the National Academy of Sciences.

[22]  A. Dell,et al.  Histo-Blood Group Antigens Act as Attachment Factors of Rabbit Hemorrhagic Disease Virus Infection in a Virus Strain-Dependent Manner , 2011, PLoS pathogens.

[23]  Katalin Csill'ery,et al.  abc: an R package for approximate Bayesian computation (ABC) , 2011, 1106.2793.

[24]  Leslie A. Real,et al.  Strong seasonality produces spatial asynchrony in the outbreak of infectious diseases , 2011, Journal of The Royal Society Interface.

[25]  Toke Thomas Høye,et al.  The effects of phenological mismatches on demography , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[26]  L. Capucci,et al.  The non-pathogenic Australian lagovirus RCV-A1 causes a prolonged infection and elicits partial cross-protection to rabbit haemorrhagic disease virus. , 2010, Virology.

[27]  Louie H. Yang,et al.  Phenology, ontogeny and the effects of climate change on the timing of species interactions. , 2010, Ecology letters.

[28]  Alex R Cook,et al.  The International Journal of Biostatistics Inference in Epidemic Models without Likelihoods , 2011 .

[29]  P. Ferreras,et al.  European rabbit population trends and associated factors: a review of the situation in the Iberian Peninsula , 2009 .

[30]  E. Revilla,et al.  Breeding like rabbits: global patterns of variability and determinants of European wild rabbit reproduction , 2009 .

[31]  David Welch,et al.  Approximate Bayesian computation scheme for parameter inference and model selection in dynamical systems , 2009, Journal of The Royal Society Interface.

[32]  K. Koelle,et al.  Capturing escape in infectious disease dynamics. , 2008, Trends in ecology & evolution.

[33]  J Elith,et al.  A working guide to boosted regression trees. , 2008, The Journal of animal ecology.

[34]  K. Kovařčík,et al.  Characterisation of immunosuppression in rabbits after infection with myxoma virus. , 2008, Veterinary microbiology.

[35]  T. Boulinier,et al.  Maternal transfer of antibodies: raising immuno-ecology issues. , 2008, Trends in ecology & evolution.

[36]  M. Keeling,et al.  Modeling Infectious Diseases in Humans and Animals , 2007 .

[37]  David J D Earn,et al.  Epidemiological effects of seasonal oscillations in birth rates. , 2007, Theoretical population biology.

[38]  David N Fisman,et al.  Seasonality of infectious diseases. , 2007, Annual review of public health.

[39]  Mark M. Tanaka,et al.  Sequential Monte Carlo without likelihoods , 2007, Proceedings of the National Academy of Sciences.

[40]  D. Pontier,et al.  The role of maternal antibodies in the emergence of severe disease as a result of fragmentation , 2007, Journal of The Royal Society Interface.

[41]  M. Langlais,et al.  Waning of maternal immunity and the impact of diseases: the example of myxomatosis in natural rabbit populations. , 2006, Journal of theoretical biology.

[42]  C. Calvete Modeling the Effect of Population Dynamics on the Impact of Rabbit Hemorrhagic Disease , 2006, Conservation biology : the journal of the Society for Conservation Biology.

[43]  P. Hosseini,et al.  Seasonality and the dynamics of infectious diseases. , 2006, Ecology letters.

[44]  M. S. Sánchez,et al.  Should we expect population thresholds for wildlife disease? , 2005, Trends in ecology & evolution.

[45]  J. Greenman,et al.  The effect of seasonal host birth rates on population dynamics: the importance of resonance. , 2004, Journal of theoretical biology.

[46]  Heiko G. Rödel,et al.  Density‐dependent reproduction in the European rabbit: a consequence of individual response and age‐dependent reproductive performance , 2004 .

[47]  O. Pybus,et al.  Unifying the Epidemiological and Evolutionary Dynamics of Pathogens , 2004, Science.

[48]  D. Balding,et al.  Approximate Bayesian computation in population genetics. , 2002, Genetics.

[49]  O. Bjørnstad,et al.  DYNAMICS OF MEASLES EPIDEMICS: SCALING NOISE, DETERMINISM, AND PREDICTABILITY WITH THE TSIR MODEL , 2002 .

[50]  P. Ud,et al.  Epidemiological consequences of a pathogen having both virulent and avirulent modes of transmission: the case of rabbit haemorrhagic disease virus , 2002 .

[51]  D. Peacock,et al.  Emerging epidemiological patterns in rabbit haemorrhagic disease, its interaction with myxomatosis, and their effects on rabbit populations in South Australia , 2002 .

[52]  W. J. Müller,et al.  Statistical models for the effect of age and maternal antibodies on the development of rabbit haemorrhagic disease in Australian wild rabbits , 2002 .

[53]  Frank Fenner,et al.  Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand , 2002 .

[54]  Donald L. DeAngelis,et al.  An individual-based model of rabbit viral haemorrhagic disease in European wild rabbits (Oryctolagus cuniculus) , 2001 .

[55]  E. Gould,et al.  The emergence of rabbit haemorrhagic disease virus: will a non-pathogenic strain protect the UK? , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  B T Grenfell,et al.  Noisy Clockwork: Time Series Analysis of Population Fluctuations in Animals , 2001, Science.

[57]  J. Le Pendu,et al.  Binding of Rabbit Hemorrhagic Disease Virus to Antigens of the ABH Histo-Blood Group Family , 2000, Journal of Virology.

[58]  Gary C. White,et al.  Seasonal Compensation of Predation and Harvesting , 1999 .

[59]  M. Keeling,et al.  Patterns of density dependence in measles dynamics , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[60]  R R Kao,et al.  The dynamics of an infectious disease in a population with birth pulses. , 1998, Mathematical biosciences.

[61]  Steven A. Frank,et al.  Models of Parasite Virulence , 1996, The Quarterly Review of Biology.

[62]  S. Levin,et al.  A simulation model of the population dynamics and evolution of myxomatosis. , 1990 .

[63]  M. Stein Large sample properties of simulations using latin hypercube sampling , 1987 .

[64]  I. Parer,et al.  Comparative Dynamics of Australasian Rabbit-Populations , 1987 .

[65]  C. Krebs,et al.  On the reliability of enumeration for mark and recapture census of voles , 1976 .

[66]  M. Bartlett Measles Periodicity and Community Size , 1957 .