Infectious disease and group size: More than just a numbers game

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1669, 2015, Pages

  Nunn, Charles L ^a,b   Jordan, Ferenc ^c,d   Mc Cabe, Collin M ^e   Verdolin, Jennifer L ^a   Fewell, Jennifer H ^f  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TRENTO   (Italy)

^d MTA CENTRE FOR ECOLOGICAL RESEARCH   (Hungary)

^e HARVARD UNIVERSITY   (United States)

^f ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Comparative analysis; Infectious disease; Meta analysis; Social network; Social structure; Sociality

Indexed keywords

COMPARATIVE STUDY; DISEASE SPREAD; GROUP SIZE; INFECTIOUS DISEASE; INVERTEBRATE; META-ANALYSIS; SOCIAL NETWORK; SOCIAL STRUCTURE; VERTEBRATE;

INVERTEBRATA; VERTEBRATA;

ANIMAL; ANIMAL BEHAVIOR; BIOLOGICAL MODEL; COMMUNICABLE DISEASES; INVERTEBRATE; META ANALYSIS; POPULATION DENSITY; RISK FACTOR; SOCIAL BEHAVIOR; SPECIES DIFFERENCE; TRANSMISSION; VERTEBRATE;

ANIMALS; BEHAVIOR, ANIMAL; COMMUNICABLE DISEASES; INVERTEBRATES; MODELS, BIOLOGICAL; POPULATION DENSITY; RISK FACTORS; SOCIAL BEHAVIOR; SPECIES SPECIFICITY; VERTEBRATES;

EID: 84927739357     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0111     Document Type: Article

References (73)

1. Freeland WJ. 1979 Primate social groups as biological islands. Ecology 60, 719-728. (doi:10. 2307/1936609)
2. Møller AP, Dufva R, Allander K. 1993 Parasites and the evolution of host social behavior. Adv. Stud. Behav. 22, 65-102. (doi:10.1016/S0065-3454(08)60405-2)
3. Loehle C. 1995 Social barriers to pathogen transmission in wild animal populations. Ecology 76, 326-335. (doi:10.2307/1941192)
4. Altizer S et al. 2003 Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu. Rev. Ecol. Evol. Syst. 34, 517-547. (doi:10.1146/annurev.ecolsys.34.030102. 151725)
5. Whiteman NK, Parker PG. 2004 Effects of host sociality on ectoparasite population biology. J. Parasitol. 90, 939-947. (doi:10.1645/ GE-310R)
6. Ezenwa VO. 2004 Host social behavior and parasitic infection: a multifactorial approach. Behav. Ecol. 15, 446-454. (doi:10.1093/beheco/arh028)
7. Davies CR, Ayres JM, Dye C, Deane LM. 1991 Malaria infection rate of Amazonian primates increases with body weight and group size. Funct. Ecol. 5, 655-662. (doi:10.2307/2389485)
8. Nunn CL, Heymann EW. 2005 Malaria infection and host behaviour: a comparative study of Neotropical primates. Behav. Ecol. Sociobiol. 59, 30-37. (doi:10. 1007/s00265-005-0005-z)
9. Wlasiuk G, Khan S, Switzer W, Nachman M. 2010 A history of recurrent positive selection at the tolllike receptor 5 in primates. Mol. Biol. Evol. 26, 937-949. (doi:10.1093/molbev/msp018)
10. Arnold W, Lichtenstein AV. 1993 Ectoparasite loads decrease the fitness of alpine marmots (Marmota marmota) but are not a cost of sociality. Behav. Ecol. 4, 36-39. (doi:10.1093/ beheco/4.1.36)
11. Nunn CL, Gittleman JL, Antonovics J. 2000 Promiscuity and the primate immune system. Science 290, 1168-1170. (doi:10.1126/science.290. 5494.1168)
12. Nunn CL. 2002 A comparative study of leukocyte counts and disease risk in primates. Evolution 56, 177-190. (doi:10.1111/j.0014-3820.2002. tb00859.x)
13. Semple S, Cowlishaw G, Bennett PM. 2002 Immune system evolution among anthropoid primates: parasites, injuries and predators. Proc. R. Soc. Lond. B 269, 1031-1037. (doi:10.1098/rspb.2001.1950)
14. Naug D, Camazine S. 2002 The role of colony organization on pathogen transmission in social insects. J. Theor. Biol. 215, 427-439. (doi:10.1006/ jtbi.2001.2524)
15. Schmid-Hempel P. 1998 Parasites in social insects. Princeton, NJ: Princeton University Press.
16. Meunier J. 2015 Social immunity and the evolution of group living in insects. Phil. Trans. R. Soc. B 370, 20140102. (doi:10.1098/rstb.2014.0102)
17. Theis FJ, Ugelvig LV, Marr C, Cremer S. 2015 Opposing effects of allogrooming on disease transmission in ant societies. Phil. Trans. R. Soc. B 370, 20140108. (doi:10.1098/rstb.2014.0108)
18. Otterstatter MC, Thomson JD. 2007 Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies. Oecologia 154, 411-421. (doi:10.1007/ s00442-007-0834-8)
19. Rosengaus RB, Maxmen AB, Coates LE, Traniello JF. 1998 Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae). Behav. Ecol. Sociobiol. 44, 125-134. (doi:10.1007/s002650050523)
20. Eischen FA. 1987 Overwintering performance of honey bee colonies heavily infested with Acarapis woodi (Rennie). Apidologie 18, 293-304. (doi:10. 1051/apido:19870401)
21. Jeffree E, Allen D. 1956 The influence of colony size and of nosema disease on the rate of population loss in honey bee colonies in winter 1. J. Econ. Entomol. 49, 831-834. (doi:10.1093/jee/49.6.831)
22. Mooring MS, Hart BL. 1992 Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behaviour 123, 173-193. (doi:10.1163/156853992X00011)
23. Côté IM, Poulin R. 1995 Parasitism and group size in social animals: a meta-analysis. Behav. Ecol. 6, 159-165. (doi:10.1093/beheco/6.2.159)
24. Rubenstein DI, Hohmann ME. 1989 Parasites and social behavior of island feral horses. Oikos 55, 312-320. (doi:10.2307/3565589)
25. Bordes F, Blumstein DT, Morand S. 2007 Rodent sociality and parasite diversity. Biol. Lett. 3, 692-694. (doi:10.1098/rsbl.2007.0393)
26. Rifkin J, Nunn CL, Garamszegi LZ. 2012 Do animals living in larger groups experience greater parasitism? A meta-analysis. Am. Nat. 180, 70-82. (doi:10.1086/666081)
27. Patterson JEH, Ruckstuhl KE. 2013 Parasite infection and host group size: a meta-analytical review. Parasitology 140, 803-813. (doi:10.1017/ S0031182012002259)
28. Cohen J. 1988 Statistical power analysis for the behavioral sciences, 2nd edn. Hillsdale, NJ: Erlbaum Associates.
29. Griffin R, Nunn CL. 2011 Community structure and the spread of infectious disease in primate social networks. Evol. Ecol. 26, 779-800. (doi:10.1007/ s10682-011-9526-2)
30. Salathe M, Jones JH. 2010 Dynamics and control of diseases in networks with community structure. PLoS Comput. Biol. 6, e1000736. (doi:10.1371/ journal.pcbi.1000736)
31. Rushmore J, Caillaud D, Hall RJ, Stumpf RM, Meyers LA, Altizer S. 2014 Network-based vaccination improves prospects for disease control in wild chimpanzees. J. R. Soc. Interface 11, 20140349. (doi:10.1098/rsif.2014.0349)
32. Carne C, Semple S, Morrogh-Bernard H, Zuberbühler K, Lehmann J. 2014 the risk of disease to great apes: simulating disease spread in orang-utan (Pongo pygmaeus wurmbii) and chimpanzee (Pan troglodytes schweinfurthii) association networks. PLoS ONE 9, e95039. (doi:10.1371/journal.pone.0095039)
33. Nunn CL. 2011 The comparative approach in evolutionary anthropology and biology. Chicago, IL: University of Chicago Press.
34. Garamszegi LZ. 2014 Modern phylogenetic comparative methods and their application in evolutionary biology. Berlin, Germany: Springer.
35. Craft ME. 2015 Infectious disease transmission and contact networks in wildlife and livestock. Phil. Trans. R. Soc. B 370, 20140107. (doi:10.1098/rstb. 2014.0107)
36. Newman ME. 2006 Modularity and community structure in networks. Proc. Natl Acad. Sci. USA 103, 8577-8582. (doi:10.1073/pnas.0601602103)
37. Kreimer A, Borenstein E, Gophna U, Ruppin E. 2008 The evolution of modularity in bacterial metabolic networks. Proc. Natl Acad. Sci. USA 105, 6976-6981. (doi:10.1073/pnas.0712149105)
38. R Development Core Team. 2014 R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
39. Csardi G, Nepusz T. 2006 The igraph software package for complex network research. InterJournal Complex Syst. 1695.
40. Newman ME, Watts DJ. 1999 Scaling and percolation in the small-world network model. Phys. Rev. E 60, 7332. (doi:10.1103/PhysRevE.60.7332)
41. Naug D. 2008 Structure of the social network and its influence on transmission dynamics in a honeybee colony. Behav. Ecol. Sociobiol. 62, 1719-1725. (doi:10.1007/s00265-008-0600-x)
42. Borgatti SP, Everett MG, Freeman LC. 2002 UCINET for WINDOWS: software for social network analysis. Lexington, KY: Analytic Technologies.
43. Opsahl T, Agneessens F, Skvoretz J. 2010 Node centrality in weighted networks: Generalizing degree and shortest paths. Soc. Netw. 32, 245-251. (doi:10.1016/j.socnet.2010.03.006)
44. Dijkstra EW. 1959 A note on two problems in connexion with graphs. Numer. Math. 1, 269-271. (doi:10.1007/BF01386390)
45. Opsahl T. 2009 Structure and evolution of weighted networks. London, UK: Queen Mary University of London.
46. Bonabeau E, Dagorn L, Freon P. 1999 Scaling in animal group-size distributions. Proc. Natl Acad. Sci. USA 96, 4472-4477. (doi:10.1073/pnas.96.8.4472)
47. Kasper C, Voelkl B. 2009 A social network analysis of primate groups. Primates 50, 343-356. (doi:10. 1007/s10329-009-0153-2)
48. Borenstein M, Hedges L, Higgins J, Rothstein H. 2005 Comprehensive meta-analysis, 2nd edn. Englewood, NJ: Biostat.
49. Lajeunesse M. 2009 Meta Analysis and the Comparative Phylogenetic Method. Am. Nat. 174, 369-381. (doi:10.1086/603628)
50. Lajeunesse MJ. 2011 phyloMeta: a program for phylogenetic comparative analyses with metaanalysis. Bioinformatics 27, 2603-2604. (doi:10. 1093/bioinformatics/btr438)
51. Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N. 2011 caper: comparative analyses of phylogenetics and evolution in R. See http://RForge. R-project.org/projects/caper/.
52. Pagel M. 1999 Inferring the historical patterns of biological evolution. Nature 401, 877-884. (doi:10. 1038/44766)
53. Freckleton RP, Harvey PH, Pagel M. 2002 Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712-726. (doi:10.1086/343873)
54. Bininda-Emonds ORP et al. 2007 The delayed rise of present-day mammals. Nature 446, 507-512. (doi:10.1038/nature05634)
55. Hedges SB, Dudley J, Kumar S. 2006 TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22, 2971-2972. (doi:10. 1093/bioinformatics/btl505)
56. Brady SG, Schultz TR, Fisher BL, Ward PS. 2006 Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc. Natl Acad. Sci. USA 103, 18 172-18 177. (doi:10.1073/ pnas.0605858103)
57. Nunn CL, Thrall PH, Stewart K, Harcourt AH. 2008 Emerging infectious diseases and animal social systems. Evol. Ecol. 22, 519-543. (doi:10.1007/ s10682-007-9180-x)
58. Nunn CL, Thrall PH, Bartz K, Dasgupta T, Boesch C. 2009 Do transmission mechanisms or social systems drive cultural dynamics in socially structured populations? Anim. Behav. 77, 1515-1524. (doi:10. 1016/j.anbehav.2009.02.023)
59. Seaholm SK, Ackerman E, Wu SC. 1988 Latin hypercube sampling and the sensitivity analysis of a Monte-Carlo epidemic model. Int. J. Bio-Med. Comput. 23, 97-112. (doi:10.1016/0020-7101(88)90067-0)
60. Blower SM, Dowlatabadi H. 1994 Sensitivity and uncertainty analysis of complex-models of disease transmission-an HIV model, as an example. Int. Stat. Rev. 62, 229-243. (doi:10.2307/1403510)
61. Rushton SP, Lurz PWW, Gurnell J, Fuller R. 2000 Modelling the spatial dynamics of parapoxvirus disease in red and grey squirrels: a possible cause of the decline in the red squirrel in the UK? J. Appl. Ecol. 37, 997-1012. (doi:10.1046/j.1365-2664.2000.00553.x)
62. Burnham KP, Anderson DR. 2002 Model selection and multimodel inference: a practical informationtheoretic approach. Berlin, Germany: Springer
63. Barton K. 2011 MuMIn: Multi-model inference. R package version 1.6.5. Vienna, Austria: R Foundation for Statistical Computing.
64. Fletcher TD. 2012 QuantPsyc: quantitative psychology tools. R package version 1.5. Vienna, Austria: R Foundation for Statistical Computing.
65. Gramacy RB. 2007 tgp: an R package for Bayesian nonstationary, semiparametric nonlinear regression and design by treed Gaussian process models. J. Stat. Soft. 19, 6.
66. Gramacy RB, Taddy M. 2012 Categorical inputs, sensitivity analysis, optimization and importance tempering with tgp version 2, an R package for treed Gaussian process models. J. Stat. Soft. 33, 1-48.
67. Wlasiuk G, Nachman M. 2010 Promiscuity and the rate of molecular evolution at primate immunity genes. Evolution 64, 2204-2220. (doi:10.1111/j. 1558-5646.2010.00989.x)
68. Nunn CL. 2002 Spleen size, disease risk and sexual selection: a comparative study in primates. Evol. Ecol. Res. 4, 91-107.
69. Weinstock GM et al. 2006 Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949. (doi:10.1038/nature05260)
70. Evans J et al. 2006 Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15, 645-656. (doi:10.1111/j.1365-2583. 2006.00682.x)
71. Cremer S, Armitage SA, Schmid-Hempel P. 2007 Social immunity. Curr. Biol. 17, R693-R702. (doi:10.1016/j.cub.2007.06.008)
72. Holbrook C, Eriksson T, Overson R, Gadau J, Fewell J. 2013 Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus. Insect. Soc. 60, 191-201. (doi:10. 1007/s00040-013-0282-x)
73. Nunn CL, Thrall PH, Leendertz FH, Boesch C. 2011 The spread of fecally transmitted parasites in socially-structured populations. PLoS ONE 6, e21677. (doi:10.1371/journal.pone.0021677)