Mating strategy is determinant of adenovirus prevalence in European bats

Autoři: Federica Rossetto aff001;  Maria Iglesias-Caballero aff002;  H. Christoph Liedtke aff001;  Ivan Gomez-Mestre aff001;  Jose M. Berciano aff002;  Gonzalo Pérez-Suárez aff003;  Oscar de Paz aff003;  Carlos Ibáñez aff001;  Juan E. Echevarría aff002;  Inmaculada Casas aff002;  Javier Juste aff001
Působiště autorů: Evolutionary Biology Unit, Estación Biológica Doñana (CSIC), Sevilla, Spain aff001;  National Center of Microbiology, (ISCIII), Madrid, Spain aff002;  Department of Life Sciences, University of Alcalá, Alcalá de Henares, Madrid, Spain aff003;  CIBER Epidemiology and Public Health (CIBERESP), Madrid, Spain aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


Adenoviruses are double-strained DNA viruses found in a great number of vertebrates, including humans. In order to understand their transmission dynamics, it is crucial, even from a human health perspective, to investigate how host traits influence their prevalence. Bats are important reservoirs for adenoviruses, and here we use the results of recent screenings in Western Europe to evaluate the association between characteristic traits of bat species and their probability of hosting adenoviruses, taking into account their phylogenetic relationships. Across species, we found an important phylogenetic component in the presence of adenoviruses and mating strategy as the most determinant factor conditioning the prevalence of adenoviruses across bat species. Contrary to other more stable mating strategies (e.g. harems), swarming could hinder transmission of adenoviruses since this strategy implies that contacts between individuals are too short. Alternatively, bat species with more promiscuous behavior may develop a stronger immune system. Outstandingly high prevalence of adenoviruses was reported for the Iberian species Pipistrellus pygmaeus, P. kuhlii and Nyctalus lasiopterus and we found that in the latter, males were more likely to be infected by adenoviruses than females, due to the immunosuppressing consequence of testosterone during the mating season. As a general trend across species, we found that the number of adenoviruses positive individuals was different across localities and that the difference in prevalence between populations was correlated with their geographic distances for two of the three studied bat species (P. pygmaeus and P.kuhlii). These results increase our knowledge about the transmission mechanisms of adenoviruses.

Klíčová slova:

Adenoviruses – Animal behavior – Bats – Brownian motion – Ebola virus – Europe – Fruit bats – Phylogenetics


1. Taylor LH, Latham SM, woolhouse MEJ. Risk factors for human disease emergence. Woolhouse MEJ, Dye C, editors. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences. 2001;356: 983–989. doi: 10.1098/rstb.2001.0888 11516376

2. VanderWaal KL, Ezenwa VO. Heterogeneity in pathogen transmission: mechanisms and methodology. Functional Ecology. 2016;30: 1606–1622. doi: 10.1111/1365-2435.12645

3. Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D, Karesh WB, et al. Prediction and prevention of the next pandemic zoonosis. The Lancet. 2012;380: 1956–1965. doi: 10.1016/S0140-6736(12)61684-5 23200504

4. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, Rupprecht CE. Host Phylogeny Constrains Cross-Species Emergence and Establishment of Rabies Virus in Bats. Science. 2010;329: 676–679. doi: 10.1126/science.1188836 20689015

5. Luis Angela D., Hayman David T. S., O’Shea Thomas J., Cryan Paul M., Gilbert Amy T., Pulliam Juliet R. C., et al. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proceedings of the Royal Society B: Biological Sciences. 2013;280: 20122753. doi: 10.1098/rspb.2012.2753 23378666

6. Olival KJ, Hosseini PR, Zambrana-Torrelio C, Ross N, Bogich TL, Daszak P. Host and viral traits predict zoonotic spillover from mammals. Nature. 2017;546: 646. doi: 10.1038/nature22975 28636590

7. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T. Bats: Important Reservoir Hosts of Emerging Viruses. Clinical Microbiology Reviews. 2006;19: 531–545. doi: 10.1128/CMR.00017-06 16847084

8. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, et al. Fruit bats as reservoirs of Ebola virus. Nature. 2005;438: 575. doi: 10.1038/438575a 16319873

9. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, et al. Bats Are Natural Reservoirs of SARS-Like Coronaviruses. Science. 2005;310: 676–679. doi: 10.1126/science.1118391 16195424

10. Yob JM, Field H, Rashdi AM, Morrissy C, van der Heide B, Rota P, et al. Nipah virus infection in bats (order Chiroptera) in peninsular Malaysia. Emerging Infectious Diseases. 2001;7: 439. doi: 10.3201/eid0703.010312 11384522

11. Dobson AP. What Links Bats to Emerging Infectious Diseases? Science. 2005;310: 628–629. doi: 10.1126/science.1120872 16254175

12. Mayen F. Haematophagous Bats in Brazil, Their Role in Rabies Transmission, Impact on Public Health, Livestock Industry and Alternatives to an Indiscriminate Reduction of Bat Population. Journal of Veterinary Medicine, Series B. 2003;50: 469–472. doi: 10.1046/j.1439-0450.2003.00713.x 14720182

13. Baker ML, Schountz T, Wang L-F. Antiviral Immune Responses of Bats: A Review. Zoonoses and Public Health. 2013;60: 104–116. doi: 10.1111/j.1863-2378.2012.01528.x 23302292

14. Brook CE, Dobson AP. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends in Microbiology. 2015;23: 172–180. doi: 10.1016/j.tim.2014.12.004 25572882

15. Pozo F, Juste J, Vázquez-Morón S, Aznar-López C, Ibáñez C, Garin I, et al. Identification of Novel Betaherpesviruses in Iberian Bats Reveals Parallel Evolution. PLOS ONE. 2016;11: e0169153. doi: 10.1371/journal.pone.0169153 28036408

16. Iglesias-Caballero M, Juste J, Vázquez-Morón S, Falcon A, Aznar-Lopez C, Ibáñez C, et al. New Adenovirus Groups in Western Palaearctic Bats. Viruses. 2018;10: 443. doi: 10.3390/v10080443 30127258

17. Simmons NB. Order Chiroptera. Mammal Species of the World: A Taxonomic and Geographic Reference. 2005; 312–529.

18. Kunz TH. Roosting Ecology of Bats. In: Kunz TH, editor. Ecology of Bats. Boston, MA: Springer US; 1982. pp. 1–55.

19. Altringham JD. Bats: From Evolution to Conservation. OUP Oxford; 2011.

20. Davison AJ, Benkő M, Harrach B. Genetic content and evolution of adenoviruses. Journal of General Virology. 2003;84: 2895–2908. doi: 10.1099/vir.0.19497-0 14573794

21. Brandt CD, Kim HW, Vargosko AJ, Jeffries BC, Arrobio JO, Rindge B, et al. INFECTIONS IN 18, 000 INFANTS AND CHILDREN IN A CONTROLLED STUDY OF RESPIRATORY TRACT DISEASE. I. ADENOVIRUS PATHOGENICITY IN RELATION TO SEROLOGIC TYPE AND ILLNESS SYNDROME. Am J Epidemiol. 1969;90: 484–500. doi: 10.1093/oxfordjournals.aje.a121094 4312064

22. Khanal S, Ghimire P, Dhamoon AS. The Repertoire of Adenovirus in Human Disease: The Innocuous to the Deadly. Biomedicines. 2018;6: 30. doi: 10.3390/biomedicines6010030 29518985

23. Maeda K, Hondo E, Terakawa J, Kiso Y, Nakaichi N, Endoh D, et al. Isolation of Novel Adenovirus from Fruit Bat (Pteropus dasymallus yayeyamae). Emerg Infect Dis. 2008;14: 347–349. doi: 10.3201/eid1402.070932 18258142

24. Li Y, Ge X, Zhang H, Zhou P, Zhu Y, Zhang Y, et al. Host Range, Prevalence, and Genetic Diversity of Adenoviruses in Bats. Journal of Virology. 2010;84: 3889–3897. doi: 10.1128/JVI.02497-09 20089640

25. Sonntag M, Mühldorfer K, Speck S, Wibbelt G, Kurth A. New Adenovirus in Bats, Germany. Emerging Infectious Diseases. 2009;15: 2052. doi: 10.3201/eid1512.090646 19961700

26. Vidovszky MZ, Kohl C, Boldogh S, Görföl T, Wibbelt G, Kurth A, et al. Random sampling of the Central European bat fauna reveals the existence of numerous hitherto unknown adenoviruses+. Acta Veterinaria Hungarica. 2015; doi: 10.1556/004.2015.047 26599097

27. Musher DM. How Contagious Are Common Respiratory Tract Infections? New England Journal of Medicine. 2003;348: 1256–1266. doi: 10.1056/NEJMra021771 12660390

28. Sandrock C, Stollenwerk N. Acute Febrile Respiratory Illness in the ICU. Chest. 2008;133: 1221–1231. doi: 10.1378/chest.07-0778 18460521

29. Pica N, Bouvier NM. Environmental factors affecting the transmission of respiratory viruses. Current Opinion in Virology. 2012;2: 90–95. doi: 10.1016/j.coviro.2011.12.003 22440971

30. Kohl C, Vidovszky MZ, Mühldorfer K, Dabrowski PW, Radonić A, Nitsche A, et al. Genome Analysis of Bat Adenovirus 2: Indications of Interspecies Transmission. Journal of Virology. 2012;86: 1888–1892. doi: 10.1128/JVI.05974-11 22130531

31. Podgorski II, Pantó L, Földes K, de Winter I, Jánoska M, Sós E, et al. Adenoviruses of the most ancient primate lineages support the theory on virus–host co-evolution. Acta Veterinaria Hungarica. 2018;66: 474–487. doi: 10.1556/004.2018.042 30264611

32. Webber QMR, Fletcher QE, Willis CKR. Viral Richness is Positively Related to Group Size, but Not Mating System, in Bats. EcoHealth. 2017;14: 652–661. doi: 10.1007/s10393-017-1276-3 29030788

33. Muriel Dietrich, Teresa Kearney, Seamark Ernest C. J., Paweska Janusz T., Markotter Wanda. Synchronized shift of oral, faecal and urinary microbiotas in bats and natural infection dynamics during seasonal reproduction. Royal Society Open Science. 5: 180041. doi: 10.1098/rsos.180041 29892443

34. Dietz C, Nill D, von Helversen O. Bats of Britain, Europe and Northwest Africa. A & C Black; 2009.

35. Gannon WL, Sikes RS. Guidelines of the American Society of Mammalogists for the Use of Wild Mammals in Research. J Mammal. 2007;88: 809–823. doi: 10.1644/06-MAMM-F-185R1.1

36. Casas I, Avellon A, Mosquera M, Jabado O, Echevarria JE, Campos RH, et al. Molecular Identification of Adenoviruses in Clinical Samples by Analyzing a Partial Hexon Genomic Region. Journal of Clinical Microbiology. 2005;43: 6176–6182. doi: 10.1128/JCM.43.12.6176-6182.2005 16333124

37. Calvo C, García-García ML, Sanchez-Dehesa R, Román C, Tabares A, Pozo F, et al. Eight Year Prospective Study of Adenoviruses Infections in Hospitalized Children. Comparison with Other Respiratory Viruses. PLOS ONE. 2015;10: e0132162. doi: 10.1371/journal.pone.0132162 26147465

38. Ibáñez C, García-Mudarra JL, Ruedi M, Stadelmann B, Juste J. The Iberian contribution to cryptic diversity in European bats [Internet]. Dec 2006 [cited 1 Apr 2019].

39. Kaňuch P, Hájková P, Řehák Z, Bryja J. A rapid PCR-based test for species identification of two cryptic bats Pipistrellus pipistrellus and P. pygmaeus and its application on museum and dropping samples [Internet]. Jun 2007 [cited 1 Apr 2019].

40. Tsagkogeorga G, Parker J, Stupka E, Cotton JA, Rossiter SJ. Phylogenomic Analyses Elucidate the Evolutionary Relationships of Bats. Current Biology. 2013;23: 2262–2267. doi: 10.1016/j.cub.2013.09.014 24184098

41. Guillén-Servent A, Francis CM, Ricklefs RE. Phylogeny and biogeography of the horseshoe bats. Horseshoe bats of the world Exeter: Pelagic Publishing Ltd. 2003;

42. Ruedi M, Stadelmann B, Gager Y, Douzery EJP, Francis CM, Lin L-K, et al. Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera). Molecular Phylogenetics and Evolution. 2013;69: 437–449. doi: 10.1016/j.ympev.2013.08.011 23988307

43. Stadelmann B, Jacobs DS, Schoeman C, Ruedi M. Phylogeny of African Myotis bats (Chiroptera, Vespertilionidae) inferred from cytochrome b sequences [Internet]. Sep 2004 [cited 19 Apr 2019].

44. Hoofer SR, Bussche RAVD. Molecular Phylogenetics of the Chiropteran Family Vespertilionidae. acta. 2003;5: 1–63. doi: 10.3161/001.005.s101

45. Glez-Peñ D, Gómez-Blanco D, Reboiro-Jato M, Fdez-Riverola F, Posada D. ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Res. 2010;38: W14–W18. doi: 10.1093/nar/gkq321 20439312

46. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol. 2007;24: 1596–1599. doi: 10.1093/molbev/msm092 17488738

47. Lanfear R, Calcott B, Ho SYW, Guindon S. PartitionFinder: Combined Selection of Partitioning Schemes and Substitution Models for Phylogenetic Analyses. Mol Biol Evol. 2012;29: 1695–1701. doi: 10.1093/molbev/mss020 22319168

48. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology. 2007;7: 214. doi: 10.1186/1471-2148-7-214 17996036

49. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst Biol. 2018;67: 901–904. doi: 10.1093/sysbio/syy032 29718447

50. Fritz SA, Purvis A. Selectivity in Mammalian Extinction Risk and Threat Types: a New Measure of Phylogenetic Signal Strength in Binary Traits. Conservation Biology. 2010;24: 1042–1051. doi: 10.1111/j.1523-1739.2010.01455.x 20184650

51. Pagel M. Inferring the historical patterns of biological evolution. Nature. 1999;401: 877. doi: 10.1038/44766 10553904

52. Blomberg SP, Garland T, Ives AR. Testing for Phylogenetic Signal in Comparative Data: Behavioral Traits Are More Labile. Evolution. 2003;57: 717–745. doi: 10.1111/j.0014-3820.2003.tb00285.x 12778543

53. MARCHAIS G, THAURONT M. Action Plan for the Conservation of All Bat Species in the European Union 2018–2024. 2018.

54. R Development Core Team R. R: A language and environment for statistical computing. R foundation for statistical computing Vienna, Austria; 2011.

55. Orme D, Freckleton R, Thomas G, Petzoldt T. The caper package: comparative analysis of phylogenetics and evolution in R. R package version. 2013;5: 1–36.

56. Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution. 2012;3: 217–223.

57. Tung Ho L si, Ané C. A Linear-Time Algorithm for Gaussian and Non-Gaussian Trait Evolution Models. Syst Biol. 2014;63: 397–408. doi: 10.1093/sysbio/syu005 24500037

58. Symonds MRE, Blomberg SP. A Primer on Phylogenetic Generalised Least Squares. Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology. 2014; 105–130. doi: 10.1007/978-3-662-43550-2_5

59. Butler MA, King AA. Phylogenetic Comparative Analysis: A Modeling Approach for Adaptive Evolution. The American Naturalist. 2004;164: 683–695. doi: 10.1086/426002 29641928

60. Akaike H. A New Look at the Statistical Model Identification. Selected Papers of Hirotugu Akaike. 1974; 215–222. doi: 10.1007/978-1-4612-1694-0_16

61. Burnham KP, Anderson DR. Multimodel Inference: Understanding AIC and BIC in Model Selection. Sociological Methods & Research. 2004;33: 261–304. doi: 10.1177/0049124104268644

62. Barton K. MuMIn: multi-model inference. 2009;

63. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004;20: 289–290. doi: 10.1093/bioinformatics/btg412 14734327

64. Bates D, Sarkar D, Bates MD, Matrix L. The lme4 package. R package version. 2007;2: 74.

65. Mantel N. The Detection of Disease Clustering and a Generalized Regression Approach. Cancer Res. 1967;27: 209–220. 6018555

66. Dray S, Dufour A-B. The ade4 package: implementing the duality diagram for ecologists. Journal of statistical software. 2007;22: 1–20.

67. Lipson C. Statistical design and analysis of engineering experiments [Internet]. 1973.

68. Gervasi SS, Civitello DJ, Kilvitis HJ, Martin LB. The context of host competence: a role for plasticity in host–parasite dynamics. Trends in Parasitology. 2015;31: 419–425. doi: 10.1016/ 26048486

69. Parsons KN, Jones G, Davidson-Watts I, Greenaway F. Swarming of bats at underground sites in Britain—implications for conservation. Biological Conservation. 2003;111: 63–70. doi: 10.1016/S0006-3207(02)00250-1

70. McCracken GF, Wilkinson GS. Bat Mating Systems. In: Crichton EG, Krutzsch PH, editors. Reproductive Biology of Bats. London: Academic Press; 2000. pp. 321–362. doi: 10.1016/B978-012195670-7/50009-6

71. Nunn CL, Gittleman JL, Antonovics J. Promiscuity and the Primate Immune System. Science. 2000;290: 1168–1170. doi: 10.1126/science.290.5494.1168 11073457

72. Schneeberger K, Czirják GÁ, Voigt CC. Measures of the Constitutive Immune System Are Linked to Diet and Roosting Habits of Neotropical Bats. PLOS ONE. 2013;8: e54023. doi: 10.1371/journal.pone.0054023 23342064

73. Munster VJ, Baas C, Lexmond P, Waldenström J, Wallensten A, Fransson T, et al. Spatial, Temporal, and Species Variation in Prevalence of Influenza A Viruses in Wild Migratory Birds. PLOS Pathogens. 2007;3: e61. doi: 10.1371/journal.ppat.0030061 17500589

74. Towner JS, Pourrut X, Albariño CG, Nkogue CN, Bird BH, Grard G, et al. Marburg Virus Infection Detected in a Common African Bat. PLOS ONE. 2007;2: e764. doi: 10.1371/journal.pone.0000764 17712412

75. Hanson BA, Luttrell MP, Goekjian VH, Niles L, Swayne DE, Senne DA, et al. IS THE OCCURRENCE OF AVIAN INFLUENZA VIRUS IN CHARADRIIFORMES SPECIES AND LOCATION DEPENDENT? In: [Internet]. 30 Sep 2013 [cited 1 Apr 2019].

76. Greenwood PJ. Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour. 1980;28: 1140–1162. doi: 10.1016/S0003-3472(80)80103-5

77. Klein SL. The effects of hormones on sex differences in infection: from genes to behavior. Neuroscience & Biobehavioral Reviews. 2000;24: 627–638. doi: 10.1016/S0149-7634(00)00027-0

78. Baker KS, Suu‐Ire R, Barr J, Hayman DTS, Broder CC, Horton DL, et al. Viral antibody dynamics in a chiropteran host. Journal of Animal Ecology. 2014; 415–428. doi: 10.1111/1365-2656.12153 24111634

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