Who infects whom? Social networks and tuberculosis transmission in wild meerkats

Transmission of infectious diseases is strongly influenced by who contacts whom. Despite the global distribution of tuberculosis (TB) in free-living wild mammal populations, little is known of the mechanisms of social transmission of Mycobacterium bovis between individuals. Here, I use a network approach to examine for correlations between five distinct types of intra- and intergroup social interaction and changes in TB status of 110 wild meerkats (Suricata suricatta) in five social groups over two years. Contrary to predictions, the most socially interactive animals were not at highest risk of acquiring infection, indicating that in addition to contact frequency, the type and direction of interactions must be considered when quantifying disease risk. Within social groups, meerkats that groomed others most were more likely to become infected than individuals who received high levels of grooming. Conversely, receiving, but not initiating, aggression was associated with M. bovis infection. Incidence of intergroup roving by male meerkats was correlated with the rovers themselves subsequently testing TB-positive, suggesting a possible route for transmission of infection between social groups. Exposure time was less important than these social interactions in influencing TB risk. This study represents a novel application of social network analysis using empirical data to elucidate the role of specific interactions in the transmission of an infectious disease in a free-living wild animal population.

[1]  L. Corner The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: how to assess the risk. , 2006, Veterinary microbiology.

[2]  Julian A. Drewe,et al.  The social network structure of a wild meerkat population: 2. Intragroup interactions , 2009, Behavioral Ecology and Sociobiology.

[3]  Menna E. Jones,et al.  Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) population: using social network analysis to reveal seasonal variability in social behaviour and its implications for transmission of devil facial tumour disease. , 2009, Ecology letters.

[4]  Francesca Cagnacci,et al.  Comparison of social networks derived from ecological data: implications for inferring infectious disease dynamics. , 2009, The Journal of animal ecology.

[5]  A Griffin,et al.  Cooperation, control, and concession in meerkat groups. , 2001, Science.

[6]  P. Morris,et al.  The transmission of Mycobacterium bovis infection to cattle. , 2003, Research in veterinary science.

[7]  R. G. Hewinson,et al.  Validation of the BrockTB Stat-Pak Assay for Detection of Tuberculosis in Eurasian Badgers (Meles meles) and Influence of Disease Severity on Diagnostic Accuracy , 2008, Journal of Clinical Microbiology.

[8]  T. Clutton‐Brock,et al.  Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal , 2007, Proceedings of the Royal Society B: Biological Sciences.

[9]  James D. Thomson,et al.  Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies , 2007, Oecologia.

[10]  R S Morris,et al.  Social-network analysis of Mycobacterium bovis transmission among captive brushtail possums (Trichosurus vulpecula). , 2003, Preventive veterinary medicine.

[11]  Joah R Madden,et al.  Manipulating grooming by decreasing ectoparasite load causes unpredicted changes in antagonism , 2009, Proceedings of the Royal Society B: Biological Sciences.

[12]  P. E. Kopp,et al.  Superspreading and the effect of individual variation on disease emergence , 2005, Nature.

[13]  N. Walker,et al.  Social organization and movement influence the incidence of bovine tuberculosis in an undisturbed high-density badger Meles meles population. , 2007, The Journal of animal ecology.

[14]  Mary Poss,et al.  Social Organization and Parasite Risk in Mammals: Integrating Theory and Empirical Studies , 2003 .

[15]  W. Edmunds,et al.  Dynamic social networks and the implications for the spread of infectious disease , 2008, Journal of The Royal Society Interface.

[16]  G. Gettinby,et al.  Social group size affects Mycobacterium bovis infection in European badgers (Meles meles). , 2009, The Journal of animal ecology.

[17]  T. Clutton‐Brock,et al.  Costs of cooperative behaviour in suricates (Suricata suricatta) , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  R. Woodroffe,et al.  Attempts to control tuberculosis in cattle by removing infected badgers: constraints imposed by live test sensitivity , 1999 .

[19]  R. Sutcliffe,et al.  Pathology of Mycobacterium bovis infection in wild meerkats (Suricata suricatta). , 2009, Journal of comparative pathology.

[20]  T. Clutton‐Brock,et al.  Intrasexual competition and sexual selection in cooperative mammals , 2006, Nature.

[21]  Stephen P. Borgatti,et al.  Centrality and network flow , 2005, Soc. Networks.

[22]  P. Hudson,et al.  The effects of social structure and sex-biased transmission on macroparasite infection , 2008, Parasitology.

[23]  J. A. Drewe,et al.  The social network structure of a wild meerkat population: 1. Inter-group interactions , 2009, Behavioral Ecology and Sociobiology.

[24]  T. Clutton‐Brock,et al.  Do meerkats engage in conflict management following aggression? Reconciliation, submission and avoidance , 2008, Animal Behaviour.

[25]  A. Michel,et al.  Accuracy of Three Diagnostic Tests for Determining Mycobacterium Bovis Infection Status in Live-Sampled Wild Meerkats (Suricata Suricatta) , 2009, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[26]  M. Keeling The implications of network structure for epidemic dynamics. , 2005, Theoretical population biology.

[27]  S. Lesellier,et al.  Development and evaluation of a gamma-interferon assay for tuberculosis in badgers (Meles meles). , 2008, Tuberculosis.

[28]  T. Clutton‐Brock,et al.  Social functions of allogrooming in cooperatively breeding meerkats , 2006, Animal Behaviour.

[29]  T. Clutton‐Brock,et al.  Dispersal, Eviction, and Conflict in Meerkats (Suricata suricatta): An Evolutionarily Stable Strategy Model , 2004, The American Naturalist.

[30]  P. Cross,et al.  Wildlife Population Structure and Parasite Transmission: Implications for Disease Management , 2009 .

[31]  L. Corner,et al.  The re-emergence of Mycobacterium bovis infection in brushtail possums (Trichosurus vulpecula) after localised possum eradication , 2003, New Zealand veterinary journal.

[32]  T. Clutton‐Brock,et al.  Infanticide and expulsion of females in a cooperative mammal , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[33]  Monika Böhm,et al.  Dynamic interactions among badgers: implications for sociality and disease transmission. , 2008, The Journal of animal ecology.

[34]  D. Macdonald,et al.  Dispersal and extra-territorial prospecting by slender-tailed meerkats (Suricata suricatta) in the south-western Kalahari , 1996 .

[35]  L. Freeman,et al.  Centrality in valued graphs: A measure of betweenness based on network flow , 1991 .

[36]  R. Hanneman Introduction to Social Network Methods , 2001 .

[37]  Nigel C. Bennett,et al.  Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats , 2006, Proceedings of the National Academy of Sciences.

[38]  R. Delahay,et al.  The spatio‐temporal distribution of Mycobacterium bovis (bovine tuberculosis) infection in a high‐density badger population , 2000 .

[39]  T. Clutton‐Brock,et al.  Trade-offs between extraterritorial prospecting and helping in a cooperative mammal , 2005, Animal Behaviour.

[40]  R. G. Hewinson,et al.  Value of existing serological tests for identifying badgers that shed Mycobacterium bovis. , 2002, Veterinary microbiology.

[41]  T. Clutton‐Brock,et al.  Aggression and submission reflect reproductive conflict between females in cooperatively breeding meerkats Suricata suricatta , 2006, Behavioral Ecology and Sociobiology.

[42]  Stanley Wasserman,et al.  Social Network Analysis: Methods and Applications , 1994, Structural analysis in the social sciences.

[43]  J. Wilesmith,et al.  Mycobacterium bovis in the European badger (Meles meles): epidemiological findings in tuberculous badgers from a naturally infected population , 1993, Epidemiology and Infection.

[44]  G. Gettinby,et al.  The prevalence, distribution and severity of detectable pathological lesions in badgers naturally infected with Mycobacterium bovis , 2007, Epidemiology and Infection.

[45]  S. Borgatti Centrality and AIDS , 1995 .

[46]  Wayne M. Getz,et al.  Duelling timescales of host movement and disease recovery determine invasion of disease in structured populations: Duelling timescales of host movement and disease recovery , 2005 .