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Infectious disease and group size: more than just a numbers game
Open accessAbstract
Increased risk of infectious disease is assumed to be a major cost of group living, yet empirical evidence for this effect is mixed. We studied whether larger social groups are more subdivided structurally. If so, the social subdivisions that form in larger groups may act as barriers to the spread of infection, weakening the association between group size and infectious disease. To investigate this ‘social bottleneck’ hypothesis, we examined the association between group size and four network structure metrics in 43 vertebrate and invertebrate species. We focused on metrics involving modularity, clustering, distance and centralization. In a meta-analysis of intraspecific variation in social networks, modularity showed positive associations with network size, with a weaker but still positive effect in cross-species analyses. Network distance also showed a positive association with group size when using intraspecific variation. We then used a theoretical model to explore the effects of subgrouping relative to other effects that influence disease spread in socially structured populations. Outbreaks reached higher prevalence when groups were larger, but subgrouping reduced prevalence. Subgrouping also acted as a ‘brake’ on disease spread between groups. We suggest research directions to understand the conditions under which larger groups become more subdivided, and to devise new metrics that account for subgrouping when investigating the links between sociality and infectious disease risk.
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“High-density living and increased contact can increase pathogen transmission rates among hosts (Nunn et al. 2015).”
From Red fox viromes in urban and rural landscapes (2020) · cites this paper as Nunn et al. 2015
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Citations
Cites
Modularity and community structure in networks
Newman, M. E. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601602103 · Cited by 12,256
The delayed rise of present-day mammals
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., & Purvis, A. (2007) · Nature · doi:10.1038/nature05634 · Cited by 2,082
Dynamics and Control of Diseases in Networks with Community Structure
Salathé, M., & Jones, J. H. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000736 · Cited by 586
Flagged first, then by citations
Research works printed but not linked: 67
- 10.2307/1936609 · DOI
- 10.1016/S0065-3454(08)60405-2 · DOI
- 10.2307/1941192 · DOI · Paper page
- 10.1146/annurev.ecolsys.34.030102.151725 · DOI
- 10.1645/GE-310R · DOI
- 10.1093/beheco/arh028 · DOI
- 10.2307/2389485 · DOI
- 10.1007/s00265-005-0005-z · DOI
- 10.1093/molbev/msp018 · DOI
- 10.1093/beheco/4.1.36 · DOI
- 10.1126/science.290.5494.1168 · DOI
- 10.1111/j.0014-3820.2002.tb00859.x · DOI
- 10.1098/rspb.2001.1950 · DOI
- 10.1006/jtbi.2001.2524 · DOI
- Schmid-Hempel P, 1998, Parasites in social insects
- 10.1098/rstb.2014.0102 · DOI
- 10.1098/rstb.2014.0108 · DOI
- 10.1007/s00442-007-0834-8 · DOI
- 10.1007/s002650050523 · DOI
- 10.1051/apido:19870401 · DOI
- 10.1093/jee/49.6.831 · DOI
- 10.1163/156853992X00011 · DOI
- 10.1093/beheco/6.2.159 · DOI
- 10.2307/3565589 · DOI
- 10.1098/rsbl.2007.0393 · DOI
- 10.1086/666081 · DOI
- 10.1017/S0031182012002259 · DOI
- Cohen J, 1988, Statistical power analysis for the behavioral sciences
- 10.1007/s10682-011-9526-2 · DOI
- 10.1098/rsif.2014.0349 · DOI
- 10.1371/journal.pone.0095039 · DOI
- 10.7208/chicago/9780226090009.001.0001 · DOI
- 10.1007/978-3-662-43550-2 · DOI · Paper page
- 10.1098/rstb.2014.0107 · DOI
- 10.1073/pnas.0712149105 · DOI
- R Development Core Team, 2014, R: A language and environment for statistical computing
- Csardi G, 2006, The igraph software package for complex network research, InterJournal Complex Syst., 1695
- 10.1103/PhysRevE.60.7332 · DOI
- 10.1007/s00265-008-0600-x · DOI
- 10.1016/j.socnet.2010.03.006 · DOI
- 10.1007/BF01386390 · DOI
- Opsahl T, 2009, Structure and evolution of weighted networks
- 10.1073/pnas.96.8.4472 · DOI
- 10.1007/s10329-009-0153-2 · DOI
- Borenstein M, 2005, Comprehensive meta-analysis
- Lajeunesse M, 2009, Meta Analysis and the Comparative Phylogenetic Method, Am. Nat., 174, 369, 10.1086/603628 · DOI
- Lajeunesse MJ, 2011, phyloMeta: a program for phylogenetic comparative analyses with meta-analysis, Bioinformatics, 27, 2603, 10.1093/bioinformatics/btr438 · DOI
- Orme D Freckleton R Thomas G Petzoldt T Fritz S& Isaac N. 2011 caper: comparative analyses of phylogenetics and evolution in R. See http://R-Forge.R-project.org/projects/caper/. · DOI
- 10.1038/44766 · DOI · Paper page
- 10.1086/343873 · DOI · Paper page
- 10.1093/bioinformatics/btl505 · DOI · Paper page
- 10.1073/pnas.0605858103 · DOI
- 10.1007/s10682-007-9180-x · DOI
- 10.1016/j.anbehav.2009.02.023 · DOI
- 10.1016/0020-7101(88)90067-0 · DOI
- 10.2307/1403510 · DOI
- 10.1046/j.1365-2664.2000.00553.x · DOI
- Burnham KP, 2002, Model selection and multimodel inference: a practical information-theoretic approach
- 10.18637/jss.v019.i09 · DOI
- Gramacy RB, 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
- Wlasiuk G, 2010, Promiscuity and the rate of molecular evolution at primate immunity genes, Evolution, 64, 2204
- Nunn CL, 2002, Spleen size, disease risk and sexual selection: a comparative study in primates, Evol. Ecol. Res., 4, 91
- 10.1038/nature05260 · DOI
- 10.1111/j.1365-2583.2006.00682.x · DOI
- 10.1016/j.cub.2007.06.008 · DOI
- 10.1007/s00040-013-0282-x · DOI
- 10.1371/journal.pone.0021677 · DOI
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Heterogeneity in pathogen transmission: mechanisms and methodology
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“…their social network, individuals may also be disproportionately important in the spread of pathogens if they occupy key positions in their network that, if disrupted, hinders dissemination of pathogens across different subgroups (Salath e & Jones 2010; VanderWaal et al. 2014b; Nunn et al. 2015).”
BackgroundBertram, M. G., Costi, M. P., Thoré, E. S. J., Sabo-Attwood, T., & Brooks, B. (2014) · Huisarts en Wetenschap · doi:10.1007/s12445-023-2271-2 · Cited by 231
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Kappeler, P. M., Cremer, S., & Nunn, C. L. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0116 · Cited by 275
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Sah, P., Leu, S., Cross, P., Hudson, P., & Bansal, S. (2017) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1613616114 · Cited by 181
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BackgroundMultilevel Organisation of Animal Sociality.
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Sosa, S., Sueur, C., & Puga‐Gonzalez, I. (2020) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.13366 · Cited by 161
Rimbach, R., Bisanzio, D., Galvis, N. F., Link, A., Fiore, A. D., & Gillespie, T. R. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0110 · Cited by 119
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Group living and pathogen infection revisited
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“Second, the effects of group living on pathogens might depend on other aspects of host behavior, physiology, life-history, or ecology [14,15].”
Balasubramaniam, K., Beisner, B., Berman, C. M., Marco, A. D., Duboscq, J., Koirala, S., Majolo, B., MacIntosh, A., McFarland, R., Molesti, S., et al. (2018) · American Journal of Primatology · doi:10.1002/ajp.22727 · Cited by 75
“modular networks (Nunn et al., 2015), we confirmed that clustering coefficient was positively correlated with network density measures across our datasets (n = 34, r = 0.”
BackgroundMethodInfluentialParasites and Their Social Hosts
Schmid‐Hempel, P. (2017) · Trends in Parasitology · doi:10.1016/j.pt.2017.01.003 · Cited by 110
Downs, C. J., Schoenle, L. A., Han, B. A., Harrison, J. F., & Martin, L. B. (2019) · Trends in Parasitology · doi:10.1016/j.pt.2018.12.002 · Cited by 84
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BackgroundSocial Information Transmission in Animals: Lessons from Studies of Diffusion
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BackgroundModeling infection transmission in primate networks to predict centrality‐based risk
Romano, V., Duboscq, J., Sarabian, C., Thomas, E., Sueur, C., & MacIntosh, A. (2016) · American Journal of Primatology · doi:10.1002/ajp.22542 · Cited by 64
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BackgroundInfluentialBehavioural ecology and infectious disease: implications for conservation of biodiversity
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Nunn, C. L., Craft, M. E., Gillespie, T. R., Schaller, M., & Kappeler, P. M. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0115 · Cited by 59
“Many of these links have epidemiological implications, resulting in increased spread of infectious diseases through social contact patterns [1–4] and effects of infectious disease on host behaviour [2].”
BackgroundResultInfluentialSelf-citationRed fox viromes in urban and rural landscapes
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BackgroundMethodResultInfluentialFountain-Jones, N. M., Machado, G., Carver, S., Packer, C., Recamonde-Mendoza, M., & Craft, M. E. (2019) · bioRxiv · doi:10.1101/569012 · Cited by 45
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BackgroundContact networks structured by sex underpin sex‐specific epidemiology of infection
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BackgroundHawley, D. M., Gibson, A. K., Townsend, A. K., Craft, M. E., & Stephenson, J. F. (2020) · Parasitology · doi:10.1017/s0031182020002048 · Cited by 48
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BackgroundInfluentialSueur, C., Romano, V., Sosa, S., & Puga‐Gonzalez, I. (2018) · Primates · doi:10.1007/s10329-018-0682-7 · Cited by 51
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BackgroundBora, M., Bora, D., Manu, M., Barman, N., Dutta, L., Kumar, P. P., Poovathikkal, S., Suresh, K., & Nimmanapalli, R. (2020) · Pathogens · doi:10.3390/pathogens9121044 · Cited by 35
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BackgroundDrivers and consequences of variation in individual social connectivity
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BackgroundOlival, K., Latinne, A., Islam, A., Epstein, J., Hersch, R., Engstrand, R., Gurley, E., Amato, G., Luby, S., & Daszak, P. (2020) · Molecular Ecology · doi:10.1111/mec.15288 · Cited by 30
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ResultEvans, J., Hodgson, D. J., Boogert, N. J., & Silk, M. J. (2021) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-021-03102-4 · Cited by 30
“In species with social groups that have modular social structures (Nunn et al. 2015) such as fission-fusion societies (Lehmann et al. 2007; Ramos-Fernández and Morales 2014), we would predict conformist social learning to be more favoured than in species without these structures or sub-groupings,…”
BackgroundResultThe trade-off between information and pathogen transmission in animal societies
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“For example, researchers have examined the association between group size and social network metrics in 43 vertebrate and invertebrate species and showed that modularity, which is expected to increase in larger groups, acted as a buffer, reducing disease spread between subgroups [24].”
BackgroundFluctuating survival selection explains variation in avian group size
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How does individual variation in sociality influence fitness in prairie voles?Preprint
Sabol, A. C., Lambert, C., Keane, B., Solomon, N. G., & Dantzer, B. (2019) · bioRxiv · doi:10.1101/676858 · Cited by 27
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BackgroundBalasubramaniam, K., Beisner, B., Guan, J., Vandeleest, J. J., Hsieh, F., Atwill, E., & McCowan, B. (2018) · PeerJ · doi:10.7717/peerj.4271/supp-18 · Cited by 27
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BackgroundInfluentialModelling cetacean morbillivirus outbreaks in an endangered killer whale population
Weiss, M. N., Franks, D., Balcomb, K., Ellifrit, D., Silk, M., Cant, M., & Croft, D. (2020) · Biological Conservation · doi:10.1016/j.biocon.2019.108398 · Cited by 26
Genomic Epidemiology and Evolution of Escherichia coli in Wild Animals in Mexico
Murphy, R., Palm, M., Mustonen, V., Warringer, J., Farewell, A., Moradigaravand, D., & Parts, L. (2021) · mSphere · doi:10.1128/msphere.00738-20 · Cited by 32
“Larger social groups, as observed in 321 Carnivora, Artiodactyla and Primates in Figure S4C, is known to increase the social transmissions 322 of infectious agents in animal societies, which may facilitate the dispersion of virulence genes 323 (44).”
BackgroundMendenhall, I., Skiles, M., Neves, E. S., Borthwick, S., Low, D. H. W., Liang, B., Lee, B., Su, Y. C. F., & Smith, G. J. D. (2017) · One Health · doi:10.1016/j.onehlt.2017.10.001 · Cited by 25
“Contact rates drive infectious disease transmission and larger colony sizes may play a role in transmission [60,61] through periodic introductions of immunologically naïve individuals [46].”
Chappell, M., Buttemer, W., & Russell, A. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.144972 · Cited by 25
“…Silk et al., 2014) and by a range of ecological factors including resource availability and competition (Koenig et al., 1992; Russell, 2004), predation intensity (Elgar, 1989; Beauchamp, 2008), disease risk (Nunn et al., 2015) and climate (Jetz and Rubenstein, 2011; Cockburn and Russell, 2011).”
BackgroundInfluentialRomano, V., Lozano, S., & Fernández-Lopez-de-Pablo, J. (2020) · Biological Reviews of The Cambridge Philosophical Society · doi:10.1111/brv.12599 · Cited by 24
“Properties of the whole network might favour information transmission (e.g. density; Pasquaretta et al., 2014), reduce spreading processes (e.g. modularity; Nunn et al., 2015) or those same properties might even have dual roles regarding transmission (e.g. modularity; Romano et al., 2018).”
BackgroundResultExposure and susceptibility drive reinfection with gastrointestinal parasites in a social primate
Müller‐Klein, N., Heistermann, M., Strübe, C., Franz, M., Schülke, O., & Ostner, J. (2019) · Functional Ecology · doi:10.1111/1365-2435.13313 · Cited by 31
Formica, V., Donald, H., Marti, H., Irgebay, Z., & Brodie, E. (2020) · Journal of Animal Ecology · doi:10.1111/1365-2656.13322 · Cited by 23
Physiological and social consequences of gastrointestinal nematode infection in a nonhuman primate
Müller‐Klein, N., Heistermann, M., Strübe, C., Morbach, Z. M., Liebermann-Lilie, N. D., Franz, M., Schülke, O., & Ostner, J. (2018) · Behavioral Ecology · doi:10.1093/beheco/ary168 · Cited by 31
Kessler, S. E., Bonnell, T. R., Setchell, J. M., & Chapman, C. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-31568-2 · Cited by 24
The Behavioral Ecology of the Tibetan Macaque
Li, J.-H., Kappeler, P., & Sun, L.-X. (2020) · doi:10.1007/978-3-030-27920-2 · Cited by 23
American foulbrood in a honeybee colony: spore-symptom relationship and feedbacks
Stephan, J. G., de Miranda, J. D., & Forsgren, E. (2019) · BMC Ecology · doi:10.1186/s12898-020-00283-w · Cited by 22
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Manlove, K., Aiello, C. M., Sah, P., Cummins, B., Hudson, P., & Cross, P. (2018) · Proceedings of the Royal Society of London. Biological Sciences · doi:10.1098/rspb.2018.0670 · Cited by 22
Brookes, V., VanderWaal, K., & Ward, M. P. (2020) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2018.09.008 · Cited by 21
Sociality and tattoo skin disease among bottlenose dolphins in Shark Bay, Australia
Powell, S. N., Wallen, M. M., Miketa, M. L., Krzyszczyk, E., Foroughirad, V., Bansal, S., & Mann, J. (2020) · Behavioral Ecology · doi:10.1093/beheco/arz207 · Cited by 21
Gilbertson, M. L. J., Fountain-Jones, N., & Craft, M. E. (2018) · Behaviour · doi:10.1163/1568539x-00003471 · Cited by 21
“…contact heterogeneity include individual behavioral phenotypes (Natoli et al., 2005; Dizney & Dearing, 2013), the social structure of a population (Nunn et al., 2015; Sah et al., 2017), seasonal or temporal behavior changes (Chen et al., 2014), and behavioral responses to anthropogenic influences…”
BackgroundViral Richness is Positively Related to Group Size, but Not Mating System, in Bats
Webber, Q., Fletcher, Q., & Willis, C. (2017) · EcoHealth · doi:10.1007/s10393-017-1276-3 · Cited by 21
Lonsdorf, E., Gillespie, T. R., Wolf, T. M., Lipende, I., Raphael, J., Bakuza, J., Murray, C., Wilson, M. L., Kamenya, S., Mjungu, D., et al. (2016) · American Journal of Primatology · doi:10.1002/ajp.22562 · Cited by 21
“The size of social groups [Nunn & Heymann, 2005], subgroup structuring [Nunn et al., 2015], and position in a social network [Rimbach et al.”
BackgroundFerreira, S. C. M., Hofer, H., de Carvalho, L. M., & East, M. L. (2019) · Ecology and Evolution · doi:10.1002/ece3.5431 · Cited by 23
Larger, more connected societies of ants have a higher prevalence of viruses
Brahma, A., Leon, R., Hernández, G. L., & Wurm, Y. (2021) · Molecular Ecology · doi:10.1111/mec.16284 · Cited by 19
Hierarchical networks of food exchange in the black garden ant Lasius niger
Quque, M., Bles, O., Bénard, A., Héraud, A., Meunier, B., Criscuolo, F., Deneubourg, J., & Sueur, C. (2020) · Insect Science · doi:10.1111/1744-7917.12792 · Cited by 19
“We expected colony size to affect the network topology, as previous studies have shown that centralization and modularity increases with colony size (Pasquaretta et al., 2014; Nunn et al., 2015).”
BackgroundResultWhite, L. A., Siva-Jothy, J. A., Craft, M. E., & Vale, P. F. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2020.1653 · Cited by 14
Cowl, V. B., Jensen, K., Lea, J. M. D., Walker, S. L., & Shultz, S. (2020) · International Journal of Primatology · doi:10.1007/s10764-020-00139-6 · Cited by 18
Franz, M., Kramer-Schadt, S., Greenwood, A., & Courtiol, A. (2018) · Functional Ecology · doi:10.1111/1365-2435.13149 · Cited by 18
Infectious Disease and Grouping Patterns in Mule Deer
Salazar, M. F. M., Waldner, C., Stookey, J., & Bollinger, T. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150830 · Cited by 18
“However, empirical evidence for this feature is mixed [4, 15], and the relationships between epidemiological and ecological processes is intricate [16].”
BackgroundLocalized removal affects white‐tailed deer space use and contacts
Tosa, M. I., Schauber, E., & Nielsen, C. (2017) · doi:10.1002/jwmg.21176 · Cited by 18
“Social behavior shapes contact patterns and, as a result, disease transmission opportunities within host populations (Anderson et al. 1986, Altizer et al. 2003, Nunn et al. 2015).”
BackgroundComparative approaches in social network ecology
Albery, G. F., Bansal, S., & Silk, M. J. (2023) · Ecology Letters · doi:10.1111/ele.14345 · Cited by 20
Pathogens Shape Sex Differences in Mammalian Aging
Tidière, M., Badruna, A., Fouchet, D., Gaillard, J., Lemaitre, J., & Pontier, D. (2020) · Trends in Parasitology · doi:10.1016/j.pt.2020.05.004 · Cited by 17
“Among these traits, variation in host body size [44], mating system and sexual size dimorphism [42], MHC allelic diversity [45], geographical range [46], social group size [47], population density [48], and phylogeny [6,41] have been identified as playing a role.”
BackgroundDisease transmission in animal transfer networks
Dejene, S. W., Prins, H. H. T., HEITKÖNIG, I. M. A., & de Boer, W. F. (2016) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2016.12.017 · Cited by 26
“Network analysis has become increasingly popular to examine elationships between host contact patterns and disease trans- ission dynamics (Lindstrom et al., 2012; Makagon et al., 2012; anderWaal et al., 2013b; Nunn et al., 2015).”
BackgroundMethodInfluentialKauffman, K., Werner, C. S., Titcomb, G., Pender, M., Rabezara, J. Y., Herrera, J., Shapiro, J., Solis, A., Soarimalala, V., Tortosa, P., et al. (2022) · Journal of the Royal Society Interface · doi:10.1098/rsif.2021.0690 · Cited by 16
Self-citationHuman sickness detection is not dependent on cultural experience
Arshamian, A., Sundelin, T., Wnuk, E., O'Meara, C., Burenhult, N., Rodríguez, G. G., Lekander, M., Olsson, M., Lasselin, J., Axelsson, J., et al. (2021) · Proceedings of the Royal Society B · doi:10.1098/rspb.2021.0922 · Cited by 16
Keiser, C. N., Pinter‐Wollman, N., Ziemba, M. J., Kothamasu, K. S., & Pruitt, J. N. (2017) · Journal of Animal Ecology · doi:10.1111/1365-2656.12729 · Cited by 36
“We found that network modularity increased with group size, a trend commonly reported and often suggested to reduce parasite transmission in larger groups (Nunn et al., 2015; Sah et al., 2017).”
BackgroundZoonotic Blood-Borne Pathogens in Non-Human Primates in the Neotropical Region: A Systematic Review
Carrillo-Bilbao, G. A., Martin-Solano, S., & Saegerman, C. (2021) · Pathogens · doi:10.3390/pathogens10081009 · Cited by 20
How disease constrains the evolution of social systems
Udiani, O., & Fefferman, N. (2020) · Proceedings of the Royal Society B · doi:10.1098/rspb.2020.1284 · Cited by 15
“In a society where individuals associate in social groups, forming stable subpopulations, the likelihood of a locally transmitted infection spreading globally is low [14,29,30].”
BackgroundQuality, quantity, and the adaptive function of social relationships
Moor, D. D., & Brent, L. J. N. (2025) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2025.09.004 · Cited by 18
Functional traits linked to pathogen prevalence in wild bee communities
Figueroa, L., Compton, S., Grab, H., & Mcart, S. (2021) · Scientific Reports · doi:10.1038/s41598-021-87103-3 · Cited by 14
Mejía-Salazar, M. F., Goldizen, A., Menz, C., Dwyer, R. G., Blomberg, S., Waldner, C., Cullingham, C., & Bollinger, T. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175385 · Cited by 14
Pandey, A., Wojan, C., Feuka, A. B., Craft, M. E., Manlove, K., & Pepin, K. (2024) · Philosophical Transactions B · doi:10.1098/rstb.2022.0532 · Cited by 13
Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface
Balasubramaniam, K. N., Sueur, C., Huffman, M. A., & MacIntosh, A. J. J. (2019) · Fascinating life sciences · doi:10.1007/978-3-030-27920-2_13 · Cited by 19
Ketola, T., Briga, M., Honkola, T., & Lummaa, V. (2021) · Proceedings of the Royal Society B · doi:10.1098/rspb.2021.0356 · Cited by 12
“…size of a town is positively linked with the risk of death from infectious diseases [4 – 6], and (ii) if the division into subgroups, such as number of households and villages within a given town, decreases the number of casualties as is suggested by the ‘ social bottle-neck hypothesis ’ [2].”
BackgroundResultInfluentialArcher, E. K., Bennett, N., Faulkes, C., & Lutermann, H. (2015) · Oecologia · doi:10.1007/s00442-015-3494-0 · Cited by 12
“…study on the same primate population (Chapman et al. 2012), several other studies in primates and carnivores have provided theoretical and empirical evidence for a role of intergroup contact rates for endoparasite transmission (Walsh et al. 2009; Drewe 2010; Nunn et al. 2015; Rimbach et al. 2015).”
BackgroundHeat stress conditions affect the social network structure of free‐ranging sheep
Borthwick, Z., Quiring, K., Griffith, S., & Leu, S. (2023) · bioRxiv · doi:10.1101/2023.02.26.530064 · Cited by 10
“Regardless, a well-connected social network with low modularity also improves the spread of pathogens and parasites, which has neg - ative well-being and health consequences (Griffin & Nunn, 2012; Nunn et al., 2015 ).”
BackgroundHow Emergent Social Patterns in Allogrooming Combat Parasitic Infections
Wilson, S. N., Sindi, S. S., Brooks, H. C., Hohn, M. E., Price, C. R., Radunskaya, A., Williams, N. D., & Fefferman, N. (2020) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2020.00054 · Cited by 10
“, modularity, clustering, host density, and mating systems) (Altizer et al., 2003b; Nunn et al., 2015), the strategies proposed in the current work are not meant to capture meaningful, real-world behaviors.”
BackgroundMulti-level societies: different tasks at different social levels
Camerlenghi, E., & Papageorgiou, D. (2025) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.2023.0274 · Cited by 9
“Additionally, large social unit size poses a greater risk of infectious disease [78] and is linked to higher inequality of division of labour among members of the same social unit [79].”
Variation in local population size predicts social network structure in wild songbirds
Beck, K., Farine, D., Firth, J., & Sheldon, B. (2023) · Journal of Animal Ecology · doi:10.1111/1365-2656.14015 · Cited by 9
“Interspecies comparisons have also suggested that network fragmentation (modularity) generally increases with increasing group size (Nunn et al., 2015 ).”
BackgroundDecline and fall: The causes of group failure in cooperatively breeding meerkats
Duncan, C., Manser, M., & Clutton-Brock, T. (2021) · Ecology and Evolution · doi:10.1002/ece3.7655 · Cited by 9
“Moreover, it is hypothesized that the increasingly modular organization of larger groups could reduce disease prevalence (Nunn et al., 2015), with social clustering that could limit disease transmission being reported in meerkats (Drewe et al., 2011).”
BackgroundPoulin, R., & Filion, A. (2021) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-021-03039-8 · Cited by 9
Linking parasitism to network centrality and the impact of sampling bias in its interpretation
Xu, Z.-H., MacIntosh, A., Castellano-Navarro, A., Macanás-Martínez, E., Suzumura, T., & Duboscq, J. (2021) · bioRxiv · doi:10.1101/2021.06.07.447302 · Cited by 9
“…linked to increased parasitism, although this relationship is not always linear (Freeland, 1976; Altizer et al., 2003; Griffin and Nunn, 2012; Godfrey, 2013; Nunn et al., 2015, 2015; Romano et al., 2016; Rushmore et al., 2017; White et al., 2017; Briard and Ezenwa, 2021; Lucatelli et al., 2021).”
BackgroundSumner, K. M., McCabe, C. M., & Nunn, C. L. (2018) · Behaviour · doi:10.1163/1568539x-00003508 · Cited by 9
Self-citationInhibitory systems in brain evolution: pathways of vulnerability in neurodevelopmental disorders
Hanson, K. L., Greiner, D. M. Z., Schumann, C. M., & Semendeferi, K. (2024) · Brain Behavior and Evolution · doi:10.1159/000540865 · Cited by 5
“…between pathogen-rich environments and high social transmission of behavior and social learning has been demonstrated [167], though some of the risk associated with increased social transmission of behavior and culture may be mitigated by social subgrouping and fi ssion-fusion dynamics [168].”
Primate malarias as a model for cross-species parasite transmission
Voinson, M., Nunn, C. L., & Goldberg, A. (2022) · eLife · doi:10.7554/elife.69628 · Cited by 12
Self-citationWebber, Q., & Wal, E. V. (2020) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-020-02860-x · Cited by 8
McCabe, C. M., & Nunn, C. L. (2018) · Frontiers in Veterinary Science · doi:10.3389/fvets.2018.00071 · Cited by 8
Self-citationThe natural history of social bonds
Silk, J. (2025) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15318 · Cited by 7
Whittier, C., Nutter, F., Johnson, P. L. F., Cross, P., Lloyd-Smith, J., Slenning, B., & Stoskopf, M. (2021) · American Journal of Primatology · doi:10.1002/ajp.23350 · Cited by 7
“Increased modularity (i.e., separation of social units) has been shown to decrease pathogen spread and result in smaller outbreaks of disease in various wildlife species (Griffin & Nunn, 2012; Kurvers et al., 2014; Nunn et al., 2015; Sah et al., 2017).”
BackgroundYoung, M. J., Silk, M. J., Pritchard, A. J., & Fefferman, N. H. (2022) · Physical review. E · doi:10.1103/physreve.105.044315 · Cited by 6
“Such population level emergence of assortative mixing has important consequences for anticipating the spread of disease in a heterogeneous society, especially as homophily will also increase modularity and alter the dynamics of the spread of both disease and information [55, 56, 57, 7].”
BackgroundSocial group size influences pathogen transmission in salamanders
Ritchie, K. L., Vredenburg, V., Chaukulkar, S., Butler, H., & Zink, A. G. (2021) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-021-03057-6 · Cited by 7
Scaling of ant colony interaction networks
Toth, J. M., Fewell, J., & Waters, J. S. (2023) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2022.993627 · Cited by 6
“Notably, highly social insect colonies also show lower modularity than other animal social networks, which are generally built around maintaining individual alliances with local neighbors rather than construction around coordination of work (Waters and Fewell, 2012; Nunn et al., 2015).”
BackgroundSelf-citation
Metadata
- Authors
- Nunn, C. L., Jordán, F., McCabe, C. M., Verdolin, J. L., & Fewell, J. H.
- Affiliations
- Duke University (US)
- University of Trento (IT)
- Harvard University (US)
- Arizona State University (US)
- Corresponding author
- Nunn, Charles L.
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2015-05-26
- Volume
- 370
- Issue
- 1669
- Pages
- 20140111
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC4410377
- OpenAlex
- W1966269069
- Cited by
- 192
- References
- 0
- Citations by year
- 2026: 11 · 2025: 9 · 2024: 16 · 2023: 12 · 2022: 13 · 2021: 27 · 2020: 27 · 2019: 15 · 2018: 26 · 2017: 17 · 2016: 14 · 2015: 5
- FWCI
- 2.50
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Physical Sciences › Mathematics › Applied Mathematics › Mathematical and Theoretical Epidemiology and Ecology Models
- Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Complex Network Analysis Techniques
- Keywords
- infectious diseases, group size, social networks, network modularity, network distance, network centralization, network clustering, disease spread, sociality, animal social structure, vertebrates, invertebrates
- MeSH terms
- Animals, Behavior, Animal, Communicable Diseases, Invertebrates, Models, Biological, Population Density, Risk Factors, Social Behavior, Species Specificity, Vertebrates
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