Family level phylogenies reveal modes of macroevolution in RNA viruses

Kitchen, Andrew; Shackelton, Laura A.; Holmes, Edward C.

doi:10.1073/pnas.1011090108

Cited by 97 publications

(102 citation statements)

References 34 publications

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“…With the exception of Theilovirus, the host range of these species was expanded as a result of this virus update. A recent phylogenetic study of RNA viruses from three families and two genera other than the Picornaviridae revealed that host switching by virus species is more frequent than previously thought (38).…”

Section: Resultsmentioning

confidence: 97%

Toward Genetics-Based Virus Taxonomy: Comparative Analysis of a Genetics-Based Classification and the Taxonomy of Picornaviruses

Lauber

Gorbalenya

2012

J Virol

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bVirus taxonomy has received little attention from the research community despite its broad relevance. In an accompanying paper (C. Lauber and A. E. Gorbalenya, J. Virol. 86:3890 -3904, 2012), we have introduced a quantitative approach to hierarchically classify viruses of a family using pairwise evolutionary distances (PEDs) as a measure of genetic divergence. When applied to the six most conserved proteins of the Picornaviridae, it clustered 1,234 genome sequences in groups at three hierarchical levels (to which we refer as the "GENETIC classification"). In this study, we compare the GENETIC classification with the expert-based picornavirus taxonomy and outline differences in the underlying frameworks regarding the relation of virus groups and genetic diversity that represent, respectively, the structure and content of a classification. To facilitate the analysis, we introduce two novel diagrams. The first connects the genetic diversity of taxa to both the PED distribution and the phylogeny of picornaviruses. The second depicts a classification and the accommodated genetic diversity in a standardized manner. Generally, we found striking agreement between the two classifications on species and genus taxa. A few disagreements concern the species Human rhinovirus A and Human rhinovirus C and the genus Aphthovirus, which were split in the GENETIC classification. Furthermore, we propose a new supergenus level and universal, level-specific PED thresholds, not reached yet by many taxa. Since the species threshold is approached mostly by taxa with large sampling sizes and those infecting multiple hosts, it may represent an upper limit on divergence, beyond which homologous recombination in the six most conserved genes between two picornaviruses might not give viable progeny. R esearch in virology relies on virus taxonomy for providing a unified intellectual and practical framework for analysis, generalization, and knowledge dissemination. Despite its broad relevance, taxonomy has received relatively little attention from the research community. Virus taxonomy is developed under the direction of the Committee on Taxonomy of Viruses (ICTV) and recognizes five hierarchically arranged ranks: order, family, subfamily, genus, and species (in ascending order of intervirus similarity), with order and subfamily levels being used less commonly. Virus species are of principal importance (60), and for their demarcation the so-called polythetic species concept (3, 74) is applied. Accordingly, viruses are recognized as single species if they share a broad range of characteristics while constituting a replicating lineage that occupies a particular ecological niche (36, 75). These characteristics, so-called demarcation criteria, are devised for each genus separately and are revised periodically (16,35). To ensure that each virus is classified, they are allowed to vary greatly between and even within families, with no single unifying property being sought after (for a review, see reference 76). Consequently, virus species are operatio...

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Section: Resultsmentioning

confidence: 97%

Toward Genetics-Based Virus Taxonomy: Comparative Analysis of a Genetics-Based Classification and the Taxonomy of Picornaviruses

Lauber

Gorbalenya

2012

J Virol

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“…19 However, the lack of antibodies to BRSV and BPIV-3 in a larger sample of rats may be a further indication that rats in this population were not exposed to respiratory paramyxoviruses that may induce crossreactive antibodies to these and related viruses. 25 A recent study of 114 wild rats from New York City also did not identify paramyxoviruses. 13 In a previous study, the seroprevalence to rat coronavirus in wild rats was 92% but was only 4% to Sendai virus.…”

Section: Discussionmentioning

confidence: 99%

Respiratory Pathology and Pathogens in Wild Urban Rats (Rattus norvegicus and Rattus rattus)

Rothenburger

Himsworth

Clifford³

et al. 2015

Vet Pathol

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Norway (Rattus norvegicus) and black rats (Rattus rattus) are common peridomestic species, yet little is known about wild rat ecology, including their natural diseases. We describe gross and histological lesions in the respiratory tract of a sample of 711 wild urban rats. A subset was examined for 19 distinct categories of histological lesions in the respiratory tract. Testing for known respiratory pathogens included serology and polymerase chain reaction (PCR) of lung samples. Grossly evident lesions were rare (8/711; 1%). Upper respiratory tract inflammation was present in 93 of 107 (87%) rats and included rhinitis, submucosal and periglandular lymphoplasmacytic tracheitis, and/or tracheal intraluminal necrotic debris and was significantly associated (P < .05) with the presence of cilia-associated respiratory bacillus (CARB), Mycoplasma pulmonis, and increased body mass (odds ratio [OR] ¼ 1.09; 95% confidence interval [CI] ¼ 1.05-1.14 per 10 g). Within the lungs, peribronchiolar and/or perivascular lymphoplasmacytic cuffs were present in 152 of 199 rats (76%) and were also significantly associated (P .02) with CARB, M. pulmonis, and increased body mass (OR ¼ 1.20; 95% CI ¼ 1.14-1.27 per 10 g). Rats were frequently coinfected with M. pulmonis and CARB, and lesions associated with these pathogens were histologically indistinguishable. Pneumocystis sp was detected in 48 of 102 (47%) rats using PCR but was not significantly associated with lesions. This description of pathology in the respiratory system of wild rats demonstrates that respiratory disease is common. Although the impact of these lesions on individual and population health remains to be investigated, respiratory disease may be an important contributor to wild rat morbidity and mortality.Keywords cilia-associated respiratory bacillus; lung; Mycoplasma pulmonis, pathology; Pneumocystis; rats; Rattus norvegicus; Rattus rattus; respiratory diseases; wild Norway and black rats (Rattus norvegicus and Rattus rattus) are cosmopolitan peridomestic species that are well adapted to living in urban habitats.12 Negative impacts of rats on human society range from economic losses through agricultural crop destruction to zoonotic diseases. 12,13,22 Even though rats have lived in cities with people for centuries, many details of urban rat ecology remain unexplored. Specifically, little is known about the causes of natural morbidity and mortality in rats.The life span of wild urban rats is considerably shorter than that of laboratory rats, with few individuals living beyond 1 year of age.12 Conversely, laboratory rats live up to 3 years. 43Factors contributing to the rapid population turnover among wild rats are unclear. Due to the high fecundity of rats, predation and human rat control activities, including trapping and poisoning, have limited effects on population size. 12 Mortality associated with resource competition does not explain why mature rats die, since they would be expected to outcompete juvenile rats.12 Natural disease may be a key component to

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“…paramyxoviruses | respiratory syncytial viruses | human parainfluenza | pathogen interactions | cross-immunity R espiratory Syncytial Virus (RSV) and Human Parainfluenza Virus (HPIV), two important closely related members in the Paramyxovirus family (1), are leading causes of hospitalization in young children with community-acquired respiratory disease (2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13). Each year, they impose a huge burden on public health by demanding substantial healthcare system resources (14).…”

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confidence: 99%

Cross-immunity between strains explains the dynamical pattern of paramyxoviruses

Bhattacharyya

Gesteland

Korgenski

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Viral respiratory tract diseases pose serious public health problems. Our ability to predict and thus, be able to prepare for outbreaks is strained by the complex factors driving the prevalence and severity of these diseases. The abundance of diseases and transmission dynamics of strains are not only affected by external factors, such as weather, but also driven by interactions among viruses mediated by human behavior and immunity. To untangle the complex out-ofphase annual and biennial pattern of three common paramyxoviruses, Respiratory Syncytial Virus (RSV), Human Parainfluenza Virus (HPIV), and Human Metapneumovirus (hMPV), we adopt a theoretical approach that integrates ecological and immunological mechanisms of disease interactions. By estimating parameters from multiyear time series of laboratory-confirmed cases from the intermountain west region of the United States and using statistical inference, we show that models of immune-mediated interactions better explain the data than those based on ecological competition by convalescence. The strength of cross-protective immunity among viruses is correlated with their genetic distance in the phylogenetic tree of the paramyxovirus family.paramyxoviruses | respiratory syncytial viruses | human parainfluenza | pathogen interactions | cross-immunity

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Family level phylogenies reveal modes of macroevolution in RNA viruses

Cited by 97 publications

References 34 publications

Toward Genetics-Based Virus Taxonomy: Comparative Analysis of a Genetics-Based Classification and the Taxonomy of Picornaviruses

Toward Genetics-Based Virus Taxonomy: Comparative Analysis of a Genetics-Based Classification and the Taxonomy of Picornaviruses

Respiratory Pathology and Pathogens in Wild Urban Rats (Rattus norvegicus and Rattus rattus)

Cross-immunity between strains explains the dynamical pattern of paramyxoviruses

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