Abstract
Transmission of arthropod-borne viruses (arboviruses) involves infection and replication in both arthropod vectors and vertebrate hosts. Nearly all arboviruses are RNA viruses with high mutation frequencies, which leaves them vulnerable to genetic drift and fitness losses owing to population bottlenecks during vector infection, dissemination from the midgut to the salivary glands and transmission to the vertebrate host. However, despite these bottlenecks, they seem to avoid fitness declines that can result from Muller’s ratchet. In addition, founder effects that occur during the geographic introductions of human-amplified arboviruses, including chikungunya virus and Zika virus, can affect epidemic and endemic circulation, as well as virulence. In this Review, we discuss the role of genetic drift following population bottlenecks and founder effects in arboviral evolution and spread, and the emergence of human disease.
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References
Karabatsos, N. International Catalog of Arboviruses Including Certain Other Viruses of Vertebrates 4th edn (American Society of Tropical Medicine and Hygiene, 1985).
Bhatt, S. et al. The global distribution and burden of dengue. Nature 496, 504–507 (2013).
Paules, C. I. & Fauci, A. S. Yellow fever — once again on the radar screen in the Americas. N. Engl. J. Med. 376, 1397–1399 (2017).
Nwachukwu, W. E. et al. The response to re-emergence of yellow fever in Nigeria, 2017. Int. J. Infect. Dis. 92, 189–196 (2020).
Kraemer, M. U. G. et al. Spread of yellow fever virus outbreak in Angola and the Democratic Republic of the Congo 2015–16: a modelling study. Lancet Infect. Dis. 17, 330–338 (2017).
Weaver, S. C., Charlier, C., Vasilakis, N. & Lecuit, M. Zika, chikungunya, and other emerging vector-borne viral diseases. Annu. Rev. Med. 69, 395–408 (2018).
Kramer, I. M. et al. Does winter cold really limit the dengue vector Aedes aegypti in Europe? Parasites Vectors 13, 178 (2020).
Tippelt, L., Werner, D. & Kampen, H. Tolerance of three Aedes albopictus strains (Diptera: Culicidae) from different geographical origins towards winter temperatures under field conditions in northern Germany. PLoS ONE 14, e0219553 (2019).
Ko, H. Y. et al. Inter- and intra-host sequence diversity reveal the emergence of viral variants during an overwintering epidemic caused by dengue virus serotype 2 in southern Taiwan. PLoS Negl. Trop. Dis. 12, e0006827 (2018).
Domingo, E. & Holland, J. J. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51, 151–178 (1997).
Coffey, L. L. et al. Arbovirus evolution in vivo is constrained by host alternation. Proc. Natl Acad. Sci. USA 105, 6970–6975 (2008).
Deardorff, E. R. et al. West Nile virus experimental evolution in vivo and the trade-off hypothesis. PLoS Pathog. 7, e1002335 (2011).
Novella, I. S., Presloid, J. B., Smith, S. D. & Wilke, C. O. Specific and nonspecific host adaptation during arboviral experimental evolution. J. Mol. Microbiol. Biotechnol. 21, 71–81 (2011).
Forrester, N. L., Guerbois, M., Seymour, R. L., Spratt, H. & Weaver, S. C. Vector-borne transmission imposes a severe bottleneck on an RNA virus population. PLoS Pathog. 8, e1002897 (2012). This paper is one of the first to demonstrate using artificially marked arbovirus populations that the transmission cycle imposes multiple bottlenecks.
Mayr, E. Systematics and the Origin of Species (Columbia Univ. Press, 1942).
Templeton, A. R. The reality and importance of founder speciation in evolution. Bioessays 30, 470–479 (2008).
Mayr, E. in Evolution as a Process (eds Huxley, J., Hardy, A. C., & Ford E. B.) 157–180 (Princeton Univ. Press, 1954).
Muller, H. J. The relation of recombination to mutational advance. Mutat. Res. 1, 2–9 (1964).
Duarte, E., Clarke, D., Moya, A., Domingo, E. & Holland, J. Rapid fitness losses in mammalian RNA virus clones due to Muller’s ratchet. Proc. Natl Acad. Sci. USA 89, 6015–6019 (1992). This paper is the first to demonstrate Muller’s ratchet using an animal virus and an arbovirus.
Weaver, S. C., Brault, A. C., Kang, W. & Holland, J. J. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J. Virol. 73, 4316–4326 (1999).
Forrester, N. L., Coffey, L. L. & Weaver, S. C. Arboviral bottlenecks and challenges to maintaining diversity and fitness during mosquito transmission. Viruses 6, 3991–4004 (2014).
Moudy, R. M., Meola, M. A., Morin, L. L., Ebel, G. D. & Kramer, L. D. A newly emergent genotype of West Nile virus is transmitted earlier and more efficiently by Culex mosquitoes. Am. J. Trop. Med. Hyg. 77, 365–370 (2007).
Brault, A. C. et al. Venezuelan equine encephalitis emergence: enhanced vector infection from a single amino acid substitution in the envelope glycoprotein. Proc. Natl Acad. Sci. USA 101, 11344–11349 (2004).
Anishchenko, M. et al. Venezuelan encephalitis emergence mediated by a phylogenetically predicted viral mutation. Proc. Natl Acad. Sci. USA 103, 4994–4999 (2006).
Tsetsarkin, K. A. et al. Multi-peaked adaptive landscape for chikungunya virus evolution predicts continued fitness optimization in Aedes albopictus mosquitoes. Nat. Commun. 5, 4084 (2014). This paper summarizes multiple A. albopictus-adaptive mutations that accompanied the spread of the IOL into the Indian Ocean basin and Asia.
Scholle, F., Girard, Y. A., Zhao, Q., Higgs, S. & Mason, P. W. trans-Packaged West Nile virus-like particles: infectious properties in vitro and in infected mosquito vectors. J. Virol. 78, 11605–11614 (2004).
Smith, D. R., Adams, A. P., Kenney, J. L., Wang, E. & Weaver, S. C. Venezuelan equine encephalitis virus in the mosquito vector Aedes taeniorhynchus: infection initiated by a small number of susceptible epithelial cells and a population bottleneck. Virology 372, 176–186 (2008).
Kenney, J. L., Adams, A. P., Gorchakov, R., Leal, G. & Weaver, S. C. Genetic and anatomic determinants of enzootic Venezuelan equine encephalitis virus infection of Culex (Melanoconion) taeniopus. PLoS Negl. Trop. Dis. 6, e1606 (2012).
Nuckols, J. T. et al. Infection of Aedes albopictus with chikungunya virus rectally administered by enema. Vector Borne Zoonotic Dis. 13, 103–110 (2013).
Le Coupanec, A. et al. Co-infection of mosquitoes with chikungunya and dengue viruses reveals modulation of the replication of both viruses in midguts and salivary glands of Aedes aegypti mosquitoes. Int. J. Mol. Sci. 18, 1708 (2017).
Lequime, S., Fontaine, A., Ar Gouilh, M., Moltini-Conclois, I. & Lambrechts, L. Genetic drift, purifying selection and vector genotype shape dengue virus intra-host genetic diversity in mosquitoes. PLoS Genet. 12, e1006111 (2016).
Sim, S. et al. Tracking dengue virus intra-host genetic diversity during human-to-mosquito transmission. PLoS Negl. Trop. Dis. 9, e0004052 (2015).
Jupatanakul, N., Sim, S. & Dimopoulos, G. The insect microbiome modulates vector competence for arboviruses. Viruses 6, 4294–4313 (2014).
Colmant, A. M. G. et al. The recently identified flavivirus Bamaga virus is transmitted horizontally by Culex mosquitoes and interferes with West Nile virus replication in vitro and transmission in vivo. PLoS Negl. Trop. Dis. 12, e0006886 (2018).
Suzuki, Y. et al. Non-retroviral endogenous viral element limits cognate virus replication in Aedes aegypti ovaries. Curr. Biol. 30, 3495–3506.e6 (2020).
Romo, H., Kenney, J. L., Blitvich, B. J. & Brault, A. C. Restriction of Zika virus infection and transmission in Aedes aegypti mediated by an insect-specific flavivirus. Emerg. Microbes Infect. 7, 181 (2018).
Goenaga, S. et al. Potential for co-infection of a mosquito-specific flavivirus, Nhumirim virus, to block West Nile virus transmission in mosquitoes. Viruses 7, 5801–5812 (2015).
Roundy, C. M. et al. Viruses: a historical overview and recent developments. Adv. Virus Res. 98, 119–146 (2017).
Patterson, E. I. et al. Mosquito bottlenecks alter viral mutant swarm in a tissue and time-dependent manner with contraction and expansion of variant positions and diversity. Virus Evol. 4, vey001 (2018).
Karna, A. K. et al. Colonized Sabethes cyaneus, a sylvatic New World mosquito species, shows a low vector competence for Zika virus relative to Aedes aegypti. Viruses 10, 434 (2018).
Lequime, S., Richard, V., Cao-Lormeau, V. M. & Lambrechts, L. Full-genome dengue virus sequencing in mosquito saliva shows lack of convergent positive selection during transmission by Aedes aegypti. Virus Evol. 3, vex031 (2017).
Warmbrod, K. L. et al. Viral RNA-dependent RNA polymerase mutants display an altered mutation spectrum resulting in attenuation in both mosquito and vertebrate hosts. PLoS Pathog. 15, e1007610 (2019). This paper demonstrates that low-fidelity polymerase and the resultant mutant swarm of an arbovirus affect the ability to overcome bottlenecks during the transmission cycle.
Kantor, A. M., Grant, D. G., Balaraman, V., White, T. A. & Franz, A. W. E. Ultrastructural analysis of chikungunya virus dissemination from the midgut of the yellow fever mosquito, Aedes aegypti. Viruses 10, 571 (2018).
Weaver, S. C., Scott, T. W., Lorenz, L. H., Lerdthusnee, K. & Romoser, W. S. Togavirus-associated pathologic changes in the midgut of a natural mosquito vector. J. Virol. 62, 2083–2090 (1988).
Weaver, S. C. & Scott, T. W. Ultrastructural changes in the abdominal midgut of the mosquito, Culiseta melanura, during the gonotrophic cycle. Tissue Cell 22, 895–909 (1990).
Armstrong, P. M. et al. Successive blood meals enhance virus dissemination within mosquitoes and increase transmission potential. Nat. Microbiol. 5, 239–247 (2020). This paper identifies bloodmeals and the accompanying midgut stretching in the ability of arboviruses to overcome the bottleneck represented by escape from the mosquito midgut.
Stapleford, K. A. et al. Emergence and transmission of arbovirus evolutionary intermediates with epidemic potential. Cell Host Microbe 15, 706–716 (2014).
Weger-Lucarelli, J. et al. Using barcoded Zika virus to assess virus population structure in vitro and in Aedes aegypti mosquitoes. Virology 521, 138–148 (2018).
Grubaugh, N. D. et al. Genetic drift during systemic arbovirus infection of mosquito vectors leads to decreased relative fitness during host switching. Cell Host Microbe 19, 481–492 (2016). This paper demonstrates that arboviruses undergo repeated bottlenecks during spread through the mosquito vector, and the recovery of genetic diversity varies by mosquito species.
Franz, A. W., Kantor, A. M., Passarelli, A. L. & Clem, R. J. Tissue barriers to arbovirus infection in mosquitoes. Viruses 7, 3741–3767 (2015).
Ciota, A. T. et al. Quantification of intrahost bottlenecks of West Nile virus in Culex pipiens mosquitoes using an artificial mutant swarm. Infect. Genet. Evol. 12, 557–564 (2012). This paper also uses genetically marked mutant swarms to show that WNV genetic diversity declines during both mosquito midgut infection and transmission.
Dubrulle, M., Mousson, L., Moutailler, S., Vazeille, M. & Failloux, A. B. Chikungunya virus and Aedes mosquitoes: saliva is infectious as soon as two days after oral infection. PLoS ONE 4, e5895 (2009).
Smith, D. R. et al. Venezuelan equine encephalitis virus transmission and effect on pathogenesis. Emerg. Infect. Dis. 12, 1190–1196 (2006).
Vancini, R., Kramer, L. D., Ribeiro, M., Hernandez, R. & Brown, D. Flavivirus infection from mosquitoes in vitro reveals cell entry at the plasma membrane. Virology 435, 406–414 (2013).
Hanley, K. A., Azar, S. R., Campos, R. K., Vasilakis, N. & Rossi, S. L. Support for the transmission-clearance trade-off hypothesis from a study of Zika virus delivered by mosquito bite to mice. Viruses 11, 1072 (2019).
Boylan, B. T., Moreira, F. R., Carlson, T. W. & Bernard, K. A. Mosquito cell-derived West Nile virus replicon particles mimic arbovirus inoculum and have reduced spread in mice. PLoS Negl. Trop. Dis. 11, e0005394 (2017).
Aliota, M. T. et al. Molecularly barcoded Zika virus libraries to probe in vivo evolutionary dynamics. PLoS Pathog. 14, e1006964 (2018).
Grubaugh, N. D. et al. Mosquitoes transmit unique west nile virus populations during each feeding episode. Cell Rep. 19, 709–718 (2017).
Weaver, S. C., Rico-Hesse, R. & Scott, T. W. Genetic diversity and slow rates of evolution in New World alphaviruses. Curr. Top. Microbiol. Immunol. 176, 99–117 (1992).
Reisen, W. K., Fang, Y. & Brault, A. C. Limited interdecadal variation in mosquito (Diptera: Culicidae) and avian host competence for western equine encephalomyelitis virus (Togaviridae: Alphavirus). Am. J. Trop. Med. Hyg. 78, 681–686 (2008).
Bergren, N. A. et al. Western equine encephalitis virus: evolutionary analysis of a declining alphavirus based on complete genome sequences. J. Virol. 88, 9260–9267 (2014).
Bergren, N. A. et al. “Submergence” of western equine encephalitis virus: evidence of positive selection argues against genetic drift and fitness reductions. PLoS Pathog. 16, e1008102 (2020). This paper describes declines in an arbovirus fitness that were not attributed to drift or bottlenecks, and shows that fitness increased over time, suggesting ecologic explanations for the decline in enzootic transmission and human/equine cases.
Moratorio, G. & Vignuzzi, M. Monitoring and redirecting virus evolution. PLoS Pathog. 14, e1006979 (2018).
Kutchko, K. M. et al. Structural divergence creates new functional features in alphavirus genomes. Nucleic Acids Res. 46, 3657–3670 (2018).
Jaworski, E. & Routh, A. Parallel ClickSeq and nanopore sequencing elucidates the rapid evolution of defective-interfering RNAs in Flock House virus. PLoS Pathog. 13, e1006365 (2017).
Weaver, S. C. & Vasilakis, N. Molecular evolution of dengue viruses: contributions of phylogenetics to understanding the history and epidemiology of the preeminent arboviral disease. Infect. Genet. Evol. 9, 523–540 (2009).
Weaver, S. C. et al. Recombinational history and molecular evolution of western equine encephalomyelitis complex alphaviruses. J. Virol. 71, 613–623 (1997).
Lanciotti, R. S. et al. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286, 2333–2337 (1999).
Cardoso, C. W. et al. Outbreak of exanthematous illness associated with Zika, chikungunya, and dengue viruses, Salvador, Brazil. Emerg. Infect. Dis. 21, 2274–2276 (2015).
Leparc-Goffart, I., Nougairede, A., Cassadou, S., Prat, C. & de Lamballerie, X. Chikungunya in the Americas. Lancet 383, 514 (2014).
Rezza, G. et al. Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370, 1840–1846 (2007).
Venturi, G. et al. Detection of a chikungunya outbreak in central Italy, August to September 2017. Euro Surveill. 22, 17-00646 (2017).
Grubaugh, N. D. et al. Genomic epidemiology reveals multiple introductions of Zika virus into the United States. Nature 546, 401–405 (2017). This paper describes multiple introductions of ZIKV into Florida, with most quickly becoming extinct and only a few persisting for weeks to months. Whether any of the extinctions were related to founder effects remains to be determined.
Mier, Y. T.-R. L., Tatem, A. J. & Johansson, M. A. Mosquitoes on a plane: disinsection will not stop the spread of vector-borne pathogens, a simulation study. PLoS Negl. Trop. Dis. 11, e0005683 (2017).
Faria, N. R. et al. Establishment and cryptic transmission of Zika virus in Brazil and the Americas. Nature 546, 406–410 (2017).
Faria, N. R. et al. Zika virus in the Americas: early epidemiological and genetic findings. Science (2016).
Nunes, M. R. et al. Emergence and potential for spread of chikungunya virus in Brazil. BMC Med. 13, 102 (2015).
Chen, R. et al. Comprehensive genome scale phylogenetic study provides new insights on the global expansion of chikungunya virus. J. Virol. 90, 10600–10611 (2016).
Azar, S. R. et al. Differential vector competency of Aedes albopictus populations from the Americas for Zika virus. Am. J. Trop. Med. Hyg. 97, 330–339 (2017).
Roundy, C. M. et al. Variation in Aedes aegypti mosquito competence for Zika virus transmission. Emerg. Infect. Dis. 23, 625–632 (2017).
Chretien, J. P. et al. Drought-associated chikungunya emergence along coastal East Africa. Am. J. Trop. Med. Hyg. 76, 405–407 (2007).
Schuffenecker, I. et al. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med. 3, e263 (2006).
Yergolkar, P. N. et al. Chikungunya outbreaks caused by African genotype, India. Emerg. Infect. Dis. 12, 1580–1583 (2006).
Soon, Y. Y. et al. Chikungunya virus of central/east african genotype detected in Malaysia. Med. J. Malaysia 62, 214–217 (2007).
Tsetsarkin, K. A., Vanlandingham, D. L., McGee, C. E. & Higgs, S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 3, e201 (2007).
Vazeille, M. et al. Two chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PLoS ONE 2, e1168 (2007).
Langsjoen, R. M. et al. Chikungunya virus strains show lineage-specific variations in virulence and cross-protective ability in murine and nonhuman primate models. mBio 9, e02449-17 (2018).
Rezza, G. & Weaver, S. C. Chikungunya as a paradigm for emerging viral diseases: evaluating disease impact and hurdles to vaccine development. PLoS Negl. Trop. Dis. 13, e0006919 (2019).
Powers, A. M., Brault, A. C., Tesh, R. B. & Weaver, S. C. Re-emergence of chikungunya and O’nyong-nyong viruses: evidence for distinct geographical lineages and distant evolutionary relationships. J. Gen. Virol. 81, 471–479 (2000).
Yoon, I. K. et al. High rate of subclinical chikungunya virus infection and association of neutralizing antibody with protection in a prospective cohort in the Philippines. PLoS Negl. Trop. Dis. 9, e0003764 (2015).
Langsjoen, R. M. et al. Molecular virologic and clinical characteristics of a chikungunya fever outbreak in La Romana, Dominican Republic, 2014. PLoS Negl. Trop. Dis. 10, e0005189 (2016).
Bustos Carrillo, F. et al. Epidemiological evidence for lineage-specific differences in the risk of inapparent chikungunya virus infection. J. Virol. 93, e01622-18 (2019).
Chen, R., Wang, E., Tsetsarkin, K. A. & Weaver, S. C. Chikungunya virus 3′ untranslated region: adaptation to mosquitoes and a population bottleneck as major evolutionary forces. PLoS Pathog. 9, e1003591 (2013). This paper describes deleterious mutations in the 3′ UTR of the virus that apparently occurred upon introduction into Asia from Africa many decades ago and the lack of complete restoration of this fitness reduction reflected in the contemporary strain.
Stapleford, K. A. et al. Whole-genome sequencing analysis from the chikungunya virus Caribbean outbreak reveals novel evolutionary genomic elements. PLoS Negl. Trop. Dis. 10, e0004402 (2016).
de Lamballerie, X. et al. Chikungunya virus adapts to tiger mosquito via evolutionary convergence: a sign of things to come? Virol. J. 5, 33 (2008).
Kraemer, M. U. G. et al. Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat. Microbiol. 4, 854–863 (2019).
Tsetsarkin, K. A. et al. Chikungunya virus emergence is constrained in Asia by lineage-specific adaptive landscapes. Proc. Natl Acad. Sci. USA 108, 7872–7877 (2011).
Diaz-Gonzalez, E. E. et al. First report of Aedes aegypti transmission of chikungunya virus in the Americas. Am. J. Trop. Med. Hyg. 93, 1325–1329 (2015).
Haddow, A. D. et al. Genetic characterization of Zika virus strains: geographic expansion of the Asian lineage. PLoS Negl. Trop. Dis. 6, e1477 (2012).
Grard, G. et al. Zika virus in Gabon (Central Africa)—2007: a new threat from Aedes albopictus? PLoS Negl. Trop. Dis. 8, e2681 (2014).
Lanciotti, R. S. et al. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg. Infect. Dis. 14, 1232–1239 (2008).
Musso, D. & Gubler, D. J. Zika virus. Clin. Microbiol. Rev. 29, 487–524 (2016).
Liu, Y. et al. Evolutionary enhancement of Zika virus infectivity in Aedes aegypti mosquitoes. Nature 545, 482–486 (2017).
Azar, S. R., Diaz-Gonzalez, E. E., Danis-Lonzano, R., Fernandez-Salas, I. & Weaver, S. C. Naturally infected Aedes aegypti collected during a Zika virus outbreak have viral titres consistent with transmission. Emerg. Microbes Infect. 8, 242–244 (2019).
Azar, S. R. & Weaver, S. C. Vector competence: what has Zika virus taught us? Viruses 11, 867 (2019).
Liu, J. et al. Role of mutational reversions and fitness restoration in Zika virus spread to the Americas. Nat. Commun. https://doi.org/10.1038/s41467-020-20747-3 (2021).
Weger-Lucarelli, J. et al. Vector competence of American mosquitoes for three strains of Zika virus. PLoS Negl. Trop. Dis. 10, e0005101 (2016).
Smith, D. R. et al. African and Asian Zika virus isolates display phenotypic differences both in vitro and in vivo. Am. J. Trop. Med. Hyg. 98, 432–444 (2018).
Duggal, N. K. et al. Differential neurovirulence of African and Asian genotype Zika virus isolates in outbred immunocompetent mice. Am. J. Trop. Med. Hyg. 97, 1410–1417 (2017).
Marchette, N. J., Garcia, R. & Rudnick, A. Isolation of Zika virus from Aedes aegypti mosquitoes in Malaysia. Am. J. Trop. Med. Hyg. 18, 411–415 (1969).
Weaver, S. C. Host range, amplification and arboviral disease emergence. Arch. Virol. Suppl. 19, 33–44 (2005).
Shan, C. et al. A Zika virus envelope mutation preceding the 2015 epidemic enhances virulence and fitness for transmission. Proc. Natl Acad. Sci. USA 117, 20190–20197 (2020).
Vasilakis, N. et al. Potential of ancestral sylvatic dengue-2 viruses to re-emerge. Virology 358, 402–412 (2007).
Althouse, B. M. et al. Potential for Zika virus to establish a sylvatic transmission cycle in the Americas. PLoS Negl. Trop. Dis. 10, e0005055 (2016).
Young, K. I. et al. Abundance and distribution of sylvatic dengue virus vectors in three different land cover types in Sarawak, Malaysian Borneo. Parasit. Vectors 10, 406 (2017).
Swei, A., Couper, L. I., Coffey, L. L., Kapan, D. & Bennett, S. Patterns, drivers, and challenges of vector-borne disease emergence. Vector Borne Zoonotic Dis. 20, 159–170 (2020).
Guzman, M. G. et al. Dengue: a continuing global threat. Nat. Rev. Microbiol. 8, S7–S16 (2010).
Weaver, S. C., Chen, R. & Diallo, M. Chikungunya virus: role of vectors in emergence from Enzootic cycles. Annu. Rev. Entomol. 65, 313–332 (2019).
Conway, M. J., Colpitts, T. M. & Fikrig, E. Role of the vector in arbovirus transmission. Annu. Rev. Virol. 1, 71–88 (2014).
Dong, S. et al. Chikungunya virus dissemination from the midgut of Aedes aegypti is associated with temporal basal lamina degradation during bloodmeal digestion. PLoS Negl. Trop. Dis. 11, e0005976 (2017).
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
Smithburn, K. C. Neutralizing antibodies against arthropod-borne viruses in the sera of long-time residents of Malaya and Borneo. Am. J. Hyg. 59, 157–163 (1954).
Aliota, M. T. et al. Zika in the Americas, year 2: what have we learned? What gaps remain? A report from the Global Virus Network. Antivir. Res. 144, 223–246 (2017).
Cassadou, S. et al. Emergence of chikungunya fever on the French side of Saint Martin island, October to December 2013. Euro Surveill. 19, 20752 (2014).
Machado, L. C. et al. Genome sequencing reveals coinfection by multiple chikungunya virus genotypes in a recent outbreak in Brazil. PLoS Negl. Trop. Dis. 13, e0007332 (2019).
Tsetsarkin, K. A., Chen, R. & Weaver, S. C. Interspecies transmission and chikungunya virus emergence. Curr. Opin. Virol. 16, 143–150 (2016).
Acknowledgements
Research in the authors’ laboratories is supported by National Institutes of Health (NIH) grants AI120942 and AI121452 (to S.C.W.) and AI145918 (to N.V.).
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Glossary
- Zoonotic
-
Infections that spill over from non-human animals to humans.
- Enzootic
-
Ancestral, often continuous, transmission cycles of zoonotic arboviruses involving wild animals serving as amplification and/or reservoir hosts.
- Anthropophilic mosquitoes
-
Mosquitoes with a preference for and typically a tendency to bite humans.
- Mutant swarms
-
A population of RNA viruses with numerous, randomly derived mutations resulting from low-fidelity RNA replication (lack of proofreading). Mutant swarms are also termed quasispecies when they are selected and evolve as populations rather than as individual genetic variants.
- Quasispecies
-
A diverse RNA (virus) population that contains many mutants closely related to a master sequence (usually the most abundant) and selected as a population, rather than as individuals, during its evolution.
- Population bottlenecks
-
Major reductions in the population size of organisms, often used in the context of near-extinction events. Population bottlenecks result in a loss in genetic diversity and can also fix mutations at random. Population bottlenecks also represent a form of genetic drift.
- Genetic drift
-
Random changes in the genetic make-up of a population due to chance, random sampling. Drift can dominate the evolution of a virus when population sizes remain small, reducing the efficiency of selection and genetic diversity.
- Founder effects
-
The loss of genetic variation, sometimes resulting in the fixation of random mutations. Founder effects occur when a new population is established by a small number of individuals (founder population) randomly derived from a larger ancestral population. Founder effects represent a form of genetic drift.
- Muller’s ratchet
-
The step-wise fixation following population bottlenecks of random mutations, which are typically deleterious, resulting in a decline in fitness that is difficult to restore in the absence of efficient recombination.
- Vector competence
-
The intrinsic ability of an arthropod to become infected and transmit a pathogen.
- Epistasis
-
Interactions of genes or mutations such that one can suppress the effect of another on a phenotype.
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Weaver, S.C., Forrester, N.L., Liu, J. et al. Population bottlenecks and founder effects: implications for mosquito-borne arboviral emergence. Nat Rev Microbiol 19, 184–195 (2021). https://doi.org/10.1038/s41579-020-00482-8
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DOI: https://doi.org/10.1038/s41579-020-00482-8
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