Common cold viruses circulating in children threaten wild chimpanzees through asymptomatic adult carriers

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Common cold viruses circulating in children threaten wild chimpanzees through asymptomatic adult carriers
  • Williams, J. M. et al. Causes of death in the Kasekela chimpanzees of Gombe National Park, Tanzania. Am. J. Primatol. 70(8), 766–777 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Emery Thompson, M. et al. Risk factors for respiratory illness in a community of wild chimpanzees (Pan troglodytes schweinfurthii). R. Soc. Open Sci. 5(9), 18484 (2018).

    Article 

    Google Scholar 

  • Wallis, J. & Rick Lee, D. Primate conservation: The prevention of disease transmission. Int. J. Primatol. 20(6), 803–826 (1999).

    Article 

    Google Scholar 

  • Goodall, J. The Chimpanzees of Gombe: Patterns of Behavior (Belknap Press, 1986).

    Google Scholar 

  • Hastings, B., Kenny, D., Lowenstine, L. J. & Foster, J. W. Mountain gorillas and measles: Ontogeny of a wildlife vaccination program, in Proceedings of the American Association of Zoo Veterinarians Annual Meeting, 1991, no. Table 1, pp. 198–205.

  • Köndgen, S. et al. Pandemic human viruses cause decline of endangered great apes. Curr. Biol. 18(4), 260–264 (2008).

    Article 
    PubMed 

    Google Scholar 

  • Humle, T. The 2003 Epidemic of a Flu-Like Respiratory Disease at Bossou. In The Chimpanzees of Bossou and Nimba (eds Matsuzawa, T. et al.) 325–333 (Springer, 2011).

    Chapter 

    Google Scholar 

  • Kaur, T. et al. Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. Am. J. Primatol. 70(8), 755–765 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Palacios, G. et al. Human metapneumovirus infection in wild mountain Gorillas, Rwanda. Emerg. Infect. Dis. 17(4), 711–713 (2011).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Grützmacher, K. S. et al. Codetection of respiratory syncytial virus in habituated wild western lowland gorillas and humans during a respiratory disease outbreak. Ecohealth 13(3), 499–510 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mazet, J. A. K. et al. Human respiratory syncytial virus detected in mountain gorilla respiratory outbreaks. Ecohealth 17(4), 449 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Patrono, L. V. et al. Human coronavirus OC43 outbreak in wild chimpanzees, Côte d´Ivoire, 2016. Emerg. Microbes Infect. 7(1), 1–4 (2018).

    Article 

    Google Scholar 

  • Grützmacher, K. S. et al. Human respiratory syncytial virus and Streptococcus pneumoniae Infection in Wild Bonobos. Ecohealth 15(2), 462 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Köndgen, S. et al. Evidence for human Streptococcus pneumoniae in wild and captive chimpanzees: A potential threat to wild populations. Sci. Rep. 7(1), 1–8 (2017).

    Article 

    Google Scholar 

  • Scully, E. J. et al. Lethal respiratory disease associated with human rhinovirus C in Wild Chimpanzees, Uganda, 2013. Emerg. Infect. Dis. 24(2), 267–274 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Negrey, J. D. et al. Simultaneous outbreaks of respiratory disease in wild chimpanzees caused by distinct viruses of human origin. Emerg. Microbes Infect. 8(1), 139–149 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hosaka, K. Mahale: A single flu epidemic killed at least 11 chimps. Pan Afr. News 2(2), 3–4 (1995).

    Article 

    Google Scholar 

  • Szentiks, C. A., Köndgen, S., Silinski, S., Speck, S. & Leendertz, F. H. Lethal pneumonia in a captive juvenile chimpanzee (Pan troglodytes) due to human-transmitted human respiratory syncytial virus (HRSV) and infection with Streptococcus pneumoniae. J. Med. Primatol. 38(4), 236–240 (2009).

    Article 
    PubMed 

    Google Scholar 

  • Carne, C., Semple, S., Morrogh-Bernard, H., Zuberbühler, K. & Lehmann, J. 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(4), e95039 (2014).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hanamura, S. et al. Chimpanzee deaths at Mahale caused by a flu-like disease. Primates 49(1), 77–80 (2008).

    Article 
    PubMed 

    Google Scholar 

  • Patrono, L. V. et al. Monkeypox virus emergence in wild chimpanzees reveals distinct clinical outcomes and viral diversity. Nat. Microbiol. 5(7), 955–965 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Heikkinen, T. & Järvinen, A. The common cold. Lancet 361(9351), 51 (2003).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pappas, D. E. The Common Cold,” in Principles and Practice of Pediatric Infectious Diseases, Elsevier, 2018, pp. 199–202.e1.

  • Ball, T. M., Holberg, C. J., Aldous, M. B., Martinez, F. D. & Wright, A. L. Influence of attendance at day care on the common cold from birth through 13 years of age. Arch. Pediatr. Adolesc. Med. 156(2), 121–126 (2002).

    Article 
    PubMed 

    Google Scholar 

  • Byington, C. L. et al. Community surveillance of respiratory viruses among families in the Utah better identification of germs-longitudinal viral epidemiology (BIG-LoVE) study. Clin. Infect. Dis. 61(8), 1217–1224 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Monto, A. S. & Ullman, B. M. Acute respiratory illness in an american community: The Tecumseh study. JAMA 227(2), 164–169 (1974).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Birger, R. et al. Asymptomatic shedding of respiratory virus among an ambulatory population across seasons. mSphere 3(4), e00249-18 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Shaman, J. et al. Asymptomatic summertime shedding of respiratory viruses. J. Infect. Dis. 217(7), 1074–1077 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Monto, A. S. & Sullivan, K. M. Acute respiratory illness in the community. Frequency of illness and the agents involved. Epidemiol. Infect. 110(1), 145 (1993).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • O’Neill, M. B., Laval, G., Teixeira, J. C., Palmenberg, A. C. & Pepperell, C. S. Genetic susceptibility to severe childhood asthma and rhinovirus-C maintained by balancing selection in humans for 150 000 years. Hum. Mol. Genet. 29(5), 736 (2020).

    Article 
    PubMed 

    Google Scholar 

  • Bianchini, S. et al. Role of respiratory syncytial virus in pediatric pneumonia. Microorganisms 8(12), 1–14 (2020).

    Article 

    Google Scholar 

  • Gern, J. E. et al. Relationships among specific viral pathogens, virus-induced interleukin-8, and respiratory symptoms in infancy. Pediatr. Allergy Immunol. 13(6), 386–393 (2002).

    Article 
    PubMed 

    Google Scholar 

  • Coverstone, A. M. et al. Recurrent wheezing in children following human metapneumovirus infection. J. Allergy Clin. Immunol. 142(1), 297 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kermani-Alghoraishi, M., Pouramini, A., Kafi, F. & Khosravi, A. Coronavirus disease 2019 (COVID-19) and severe pericardial effusion: From pathogenesis to management: A case report based systematic review. Curr. Probl. Cardiol. 47(2), 100933 (2022).

    Article 
    PubMed 

    Google Scholar 

  • Sidhu, R. S., Sharma, A., Paterson, I. D. & Bainey, K. R. Influenza H1N1 infection leading to cardiac tamponade in a previously healthy patient: A case report. Res. Cardiovasc. Med. 5(3), 1–4 (2016).

    Google Scholar 

  • Keshavarz Valian, N., Pourakbari, B., Asna Ashari, K., Hosseinpour Sadeghi, R. & Mahmoudi, S. Evaluation of human coronavirus OC43 and SARS-COV-2 in children with respiratory tract infection during the COVID-19 pandemic. J. Med. Virol. 94(4), 1450 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kloepfer, K. M. et al. Detection of pathogenic bacteria during rhinovirus infection is associated with increased respiratory symptoms and asthma exacerbations. J. Allergy Clin. Immunol. 133(5), 1301-1307.e3 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Demuri, G. P., Gern, J. E., Eickhoff, J. C., Lynch, S. V. & Wald, E. R. Dynamics of bacterial colonization with Streptococcus pneumoniae, Haemophilus influenzae, and Moraxella catarrhalis during symptomatic and asymptomatic viral upper respiratory tract infection. Clin. Infect. Dis. 66(7), 1045 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Köster, P. C., Lapuente, J., Cruz, I., Carmena, D. & Ponce-Gordo, F. Human-borne pathogens: Are they threatening wild great ape populations?. Vet. Sci. 9(7), 356 (2022).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Dunay, E., Apakupakul, K., Leard, S., Palmer, J. L. & Deem, S. L. Pathogen transmission from humans to great apes is a growing threat to primate conservation. Ecohealth 15(1), 148–162 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Chatterjee, A., Mavunda, K. & Krilov, L. R. Current state of respiratory syncytial virus disease and management. Infect. Dis. Ther. 10(Suppl 1), 5 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Esneau, C., Duff, A. C. & Bartlett, N. W. Understanding rhinovirus circulation and impact on illness. Viruses 14(1), 141 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Simon, A., Manoha, C., Müller, A. & Schildgen, O. Human metapneumovirus and its role in childhood respiratory infections. Curr. Pediatr. Rep. 2(3), 156–165 (2014).

    Article 

    Google Scholar 

  • Morrison, R. E., Mushimiyimana, Y., Stoinski, T. S. & Eckardt, W. Rapid transmission of respiratory infections within but not between mountain gorilla groups. Sci. Rep. 11(1), 19622 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gilardi, K., et al. Best Practice Guidelines for Health Monitoring and Disease Control in Great Ape Populations. (2015).

  • Granados, A., Goodall, E. C., Luinstra, K., Smieja, M. & Mahony, J. Comparison of asymptomatic and symptomatic rhinovirus infections in university students: incidence, species diversity, and viral load. Diagn. Microbiol. Infect. Dis. 82(4), 292 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • IUCN SSC Primate Specialist Group, “Great apes, COVID-19 and the SARS CoV-2,” Apr-2021. [Online]. Available: [Accessed: 19-Apr-2023].

  • Macfie, E. J. & Williamson, E. A. Best Practice Guidelines for Great Ape Tourism. Gland, Switzerland: IUCN SSC Primate Specialist Group (2010).

  • Sundell, N. et al. PCR detection of respiratory pathogens in asymptomatic and symptomatic adults. J. Clin. Microbiol. 57(1), 10–1128 (2019).

    Article 

    Google Scholar 

  • Nuno, A. et al. Protecting great apes from disease: Compliance with measures to reduce anthroponotic disease transmission. People Nat. 4, 1387–1400 (2022).

    Article 

    Google Scholar 

  • Hartter, J. & Goldman, A. Local responses to a forest park in western Uganda: Alternate narratives on fortress conservation. Oryx 45(1), 60–68 (2011).

    Article 

    Google Scholar 

  • Jin, X. et al. Global burden of upper respiratory infections in 204 countries and territories, from 1990 to 2019. EClin. Med. 37, 100986 (2021).

    Google Scholar 

  • Chow, E. J., Uyeki, T. M. & Chu, H. Y. The effects of the COVID-19 pandemic on community respiratory virus activity. Nat. Rev. Microbiol. 21, 195–210 (2022).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Bonilla, F. A. & Oettgen, H. C. Adaptive immunity. J. Allergy Clin. Immunol. 125(2), S33–S40 (2010).

    Article 
    PubMed 

    Google Scholar 

  • Alper, C. M., Winther, B., Mandel, E. M. & Doyle, W. J. Temporal relationships for cold-like illnesses and otitis media in sibling pairs. Pediatr. Infect. Dis. J. 26(9), 778–781 (2007).

    Article 
    PubMed 

    Google Scholar 

  • Lutwama, J. J. et al. Clinic- and hospital-based sentinel influenza surveillance, Uganda 2007–2010. J. Infect. Dis. 206, S87–S93 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Ramesh, A. et al. Metagenomic next-generation sequencing of samples from pediatric febrile illness in Tororo, Uganda. PLoS ONE 14(6), e0218318 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • L’Huillier, A. G. et al. Survival of rhinoviruses on human fingers. Clin. Microbiol. Infect. 21(4), 381 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Kuehl, H. S., Elzner, C., Moebius, Y., Boesch, C. & Walsh, P. D. The price of play: Self-organized infant mortality cycles in chimpanzees. PLoS ONE 3(6), e2440 (2008).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Turner, R. B. & Lee, W.-M. Rhinovirus, in Clinical Virology, pp. 1063–1082 (2009).

  • Mäkelä, M. J. et al. Viruses and bacteria in the etiology of the common cold. J. Clin. Microbiol. 36(2), 539 (1998).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jacobs, S. E., Lamson, D. M., Kirsten, S. & Walsh, T. J. Human rhinoviruses. Clin. Microbiol. Rev. 26(1), 135–162 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Royston, L. & Tapparel, C. Rhinoviruses and respiratory enteroviruses: not as simple as ABC. Viruses 8(1), 16 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Firquet, S. et al. Survival of enveloped and non-enveloped viruses on inanimate surfaces. Microbes Environ. 30(2), 140 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Jackson, D. J. & Gern, J. E. Rhinovirus infections and their roles in asthma: Etiology and exacerbations. J. Allergy Clin. Immunol. Pract. 10(3), 673–681 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Calvo, C. et al. Respiratory syncytial virus coinfections with rhinovirus and human bocavirus in hospitalized children. Medicine (Baltimore) 94(42), e1788 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Teo, S. M. et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe 17(5), 704–715 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mysore, V. et al. Protective heterologous T cell immunity in COVID-19 induced by the trivalent MMR and Tdap vaccine antigens. Medicine 2(9), 1050-1071.e7 (2021).

    Article 
    CAS 

    Google Scholar 

  • Comunale, B. A. et al. Poliovirus vaccination induces a humoral immune response that cross reacts with SARS-CoV-2. Front. Med. 8, 710010 (2021).

    Article 

    Google Scholar 

  • Brooks, N. A. et al. The association of Coronavirus Disease-19 mortality and prior bacille Calmette–Guerin vaccination: a robust ecological analysis using unsupervised machine learning. Sci. Rep. 11(1), 774 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Winkley, K. et al. Immune cell residency in the nasal mucosa may partially explain respiratory disease severity across the age range. Sci. Rep. 11(1), 15927 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhu, Y. et al. Ancestral SARS-CoV-2, but not Omicron, replicates less efficiently in primary pediatric nasal epithelial cells. PLoS Biol. 20(8), e3001728 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Price, R. H. M., Graham, C. & Ramalingam, S. Association between viral seasonality and meteorological factors. Sci. Rep. 9(1), 1–11 (2019).

    Article 

    Google Scholar 

  • Clarke, K., Rivas, A. C., Milletich, S., Sabo-Attwood, T. & Coker, E. S. Prenatal exposure to ambient PM2.5 and early childhood growth impairment risk in east Africa. Toxics 10(11), 705 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Weary, T. E. et al. Respiratory disease patterns in rural Western Uganda, 2019–2022. Front. Pediatr. 12, 1336009 (2024).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • ECMWF, Fort Portal Weather & Climate | Temperature & Weather By Month—Climate-Data.org,” 2022. [Online]. Available: [Accessed: 27-Oct-2022].

  • Okure, D. et al. Characterization of ambient air quality in selected urban areas in Uganda using low-cost sensing and measurement technologies. Environ. Sci. Technol. 56(6), 3324–3339 (2022).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Drewe, J., O’Riain, M. J., Beamish, E., Currie, H. & Parsons, S. Survey of infections transmissible between baboons and humans, Cape Town, South Africa. Emerg. Infect. Dis. J. 18(2), 298 (2012).

    Article 

    Google Scholar 

  • Naughton-Treves, L., Treves, A., Chapman, C. A. & Wrangham, R. W. Temporal patterns of crop-raiding by primates: linking food availability in croplands and adjacent forest. J. Appl. Ecol. 35(4), 596–606 (1998).

    Article 

    Google Scholar 

  • Sarkar, D. et al. Exploring multiple dimensions of conservation success: Long-term wildlife trends, anti-poaching efforts and revenue sharing in Kibale National Park, Uganda. Anim. Conserv. 25(4), 532–549 (2022).

    Article 

    Google Scholar 

  • Wrangham, R. & Ross, E. Science and Conservation in African Forests: The Benefits of Longterm Research (Cambridge University Press, 2008).

    Book 

    Google Scholar 

  • Narat, V. et al. Higher convergence of human-great ape enteric eukaryotic viromes in central African forest than in a European zoo: A One Health analysis. Nat. Commun. 14(1), 1–13 (2023).

    Article 

    Google Scholar 

  • Negrey, J. D. et al. Viruses associated with ill health in wild chimpanzees. Am. J. Primatol. 84(2), e23358 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Teo, K. W. et al. Rhinovirus persistence during the COVID-19 pandemic—Impact on pediatric acute wheezing presentations. J. Med. Virol. 94(11), 5547–5552 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Diesner-Treiber, S. C. et al. Respiratory infections in children during a covid-19 pandemic winter. Front. Pediatr. 9, 1132 (2021).

    Article 
    ADS 

    Google Scholar 

  • Be’er, M. et al. Unforeseen changes in seasonality of pediatric respiratory illnesses during the first COVID-19 pandemic year. Pediatr. Pulmonol. 57(6), 1425–1431 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kraay, A. N. M. et al. Fomite-mediated transmission as a sufficient pathway: a comparative analysis across three viral pathogens. BMC Infect. Dis. 18(1), 1–13 (2018).

    Article 

    Google Scholar 

  • Leung, N. H. L. et al. Respiratory virus shedding in exhaled breath and efficacy of face masks. Nat. Med. 26(5), 676–680 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Reagan, K. J., McGeady, M. L. & Crowell, R. L. Persistence of human rhinovirus infectivity under diverse environmental conditions. Appl. Environ. Microbiol. 41(3), 618–620 (1981).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nuwer, R. Chimpanzees are dying from our colds—These scientists are trying to save them. Nature 625(7995), 442–446 (2024).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Cook, R. A., Karesh, W. B. & Osofsky, S. A. One world, One health: Building Interdisciplinary bridges to health in a globalized world. in One World, One Health (2004).

  • Mackenzie, J. S. & Jeggo, M. The one health approach—Why is it so important?. Trop. Med. Infect. Dis. 4(2), 88 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Köndgen, S., Schenk, S., Pauli, G., Boesch, C. & Leendertz, F. H. Noninvasive monitoring of respiratory viruses in wild chimpanzees. Ecohealth 7(3), 332–341 (2010).

    Article 
    PubMed 

    Google Scholar 

  • Forno, E. et al. Effect of vitamin D3 supplementation on severe asthma exacerbations in children with asthma and low vitamin D levels: The VDKA randomized clinical trial. JAMA 324(8), 1 (2020).

    Article 
    PubMed Central 

    Google Scholar 

  • Bochkov, Y. A., Grindle, K., Vang, F., Evans, M. D. & Gern, J. E. Improved molecular typing assay for rhinovirus species A, B, and C. J. Clin. Microbiol. 52(7), 2461–2471 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wessels, E., Schelfaut, J. J. G., Bernards, A. T. & Claas, E. C. J. Evaluation of several biochemical and molecular techniques for identification of Streptococcus pneumoniae and Streptococcus pseudopneumoniae and their detection in respiratory samples. J. Clin. Microbiol. 50(4), 1171–1177 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kaida, A. et al. Seasonal distribution and phylogenetic analysis of human metapneumovirus among children in Osaka City, Japan. J. Clin. Virol. 35(4), 394–399 (2006).

    Article 
    PubMed 

    Google Scholar 

  • Edgar, R. C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5), 1792 (2004).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 59(3), 307–321 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lefort, V., Longueville, J.-E. & Gascuel, O. SMS: Smart model selection in PhyML. Mol. Biol. Evol. 34(9), 2422–2424 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rambaut, A. FigTree, version 1.4.4 (2018).

  • Tamura, K., Stecher, G. & Kumar, S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38(7), 3022 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82(13), 1–26 (2017).

    Article 

    Google Scholar 

  • Burnham, K. P., Anderson, D. R. & Huyvaert, K. P. AIC model selection and multimodel inference in behavioral ecology: Some background, observations, and comparisons. Behav. Ecol. Sociobiol. 65(1), 23–35 (2011).

    Article 

    Google Scholar 

  • Breiman, L. Random forests. Mach. Learn. 45(1), 5–32 (2001).

    Article 

    Google Scholar 

  • Liaw, A. & Wiener, M. Classification and regression by randomForest. R. News 2(3), 18–22 (2002).

    Google Scholar 

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