Antagonistic Pleiotropy and Fitness Trade-Offs Reveal Specialist and Generalist Traits in Strains of Canine Distemper Virus
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{"title"=>"Antagonistic Pleiotropy and Fitness Trade-Offs Reveal Specialist and Generalist Traits in Strains of Canine Distemper Virus", "type"=>"journal", "authors"=>[{"first_name"=>"Veljko M.", "last_name"=>"Nikolin", "scopus_author_id"=>"16022583100"}, {"first_name"=>"Klaus", "last_name"=>"Osterrieder", "scopus_author_id"=>"7003644999"}, {"first_name"=>"Veronika", "last_name"=>"von Messling", "scopus_author_id"=>"6602433732"}, {"first_name"=>"Heribert", "last_name"=>"Hofer", "scopus_author_id"=>"7101860243"}, {"first_name"=>"Danielle", "last_name"=>"Anderson", "scopus_author_id"=>"25631949200"}, {"first_name"=>"Edward", "last_name"=>"Dubovi", "scopus_author_id"=>"7005099381"}, {"first_name"=>"Edgar", "last_name"=>"Brunner", "scopus_author_id"=>"7102511207"}, {"first_name"=>"Marion L.", "last_name"=>"East", "scopus_author_id"=>"7005670430"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"366273689", "sgr"=>"84871165634", "pmid"=>"23239996", "scopus"=>"2-s2.0-84871165634", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0050955", "issn"=>"19326203"}, "id"=>"262bfb9e-c5ca-3cf9-9373-1d80980633b9", "abstract"=>"Theoretically, homogeneous environments favor the evolution of specialists whereas heterogeneous environments favor generalists. Canine distemper is a multi-host carnivore disease caused by canine distemper virus (CDV). The described cell receptor of CDV is SLAM (CD150). Attachment of CDV hemagglutinin protein (CDV-H) to this receptor facilitates fusion and virus entry in cooperation with the fusion protein (CDV-F). We investigated whether CDV strains co-evolved in the large, homogeneous domestic dog population exhibited specialist traits, and strains adapted to the heterogeneous environment of smaller populations of different carnivores exhibited generalist traits. Comparison of amino acid sequences of the SLAM binding region revealed higher similarity between sequences from Canidae species than to sequences from other carnivore families. Using an in vitro assay, we quantified syncytia formation mediated by CDV-H proteins from dog and non-dog CDV strains in cells expressing dog, lion or cat SLAM. CDV-H proteins from dog strains produced significantly higher values with cells expressing dog SLAM than with cells expressing lion or cat SLAM. CDV-H proteins from strains of non-dog species produced similar values in all three cell types, but lower values in cells expressing dog SLAM than the values obtained for CDV-H proteins from dog strains. By experimentally changing one amino acid (Y549H) in the CDV-H protein of one dog strain we decreased expression of specialist traits and increased expression of generalist traits, thereby confirming its functional importance. A virus titer assay demonstrated that dog strains produced higher titers in cells expressing dog SLAM than cells expressing SLAM of non-dog hosts, which suggested possible fitness benefits of specialization post-cell entry. We provide in vitro evidence for the expression of specialist and generalist traits by CDV strains, and fitness trade-offs across carnivore host environments caused by antagonistic pleiotropy. These findings extend knowledge on CDV molecular epidemiology of particular relevance to wild carnivores.", "link"=>"http://www.mendeley.com/research/antagonistic-pleiotropy-fitness-tradeoffs-reveal-specialist-generalist-traits-strains-canine-distemp", "reader_count"=>127, "reader_count_by_academic_status"=>{"Unspecified"=>6, "Professor > Associate Professor"=>5, "Researcher"=>38, "Student > Doctoral Student"=>9, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>6, "Student > Master"=>20, "Other"=>9, "Student > Bachelor"=>9, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>6, "Professor > Associate Professor"=>5, "Researcher"=>38, "Student > Doctoral Student"=>9, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>6, "Student > Master"=>20, "Other"=>9, "Student > Bachelor"=>9, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>7, "Environmental Science"=>22, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>75, "Medicine and Dentistry"=>10, "Veterinary Science and Veterinary Medicine"=>1, "Physics and Astronomy"=>1, "Psychology"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>1, "Earth and Planetary Sciences"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>75}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>7}, "Environmental Science"=>{"Environmental Science"=>22}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Colombia"=>1, "Japan"=>1, "United Kingdom"=>2, "United Arab Emirates"=>1, "Portugal"=>1, "India"=>1, "Turkey"=>1, "Iran"=>1, "China"=>1, "Brazil"=>2, "Mexico"=>1, "Peru"=>1, "Germany"=>1}, "group_count"=>5}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/527287"], "description"=>"<p>(a) Phylogenetic analysis of amino acid sequences of carnivore SLAM (CD150) protein (for details see supplementary information-methods), (b) Flow cytometry analysis of parental Vero cells and derived cell lines stably expressing domestic dog, lion, and cat SLAM (CD150) receptors.</p>", "links"=>[], "tags"=>["receptors", "carnivore"], "article_id"=>197776, "categories"=>["Virology", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Veljko M. Nikolin", "Klaus Osterrieder", "Veronika von Messling", "Heribert Hofer", "Danielle Anderson", "Edward Dubovi", "Edgar Brunner", "Marion L. East"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0050955.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_SLAM_CD150_receptors_from_different_carnivore_species_/197776", "title"=>"Analysis of SLAM (CD150) receptors from different carnivore species.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-11 02:09:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/527402"], "description"=>"<p>(a) Alignment of partial SLAM binding region of CDV-H protein sequences of the strains used in this study. Amino acids 528–550 are shown, and the amino acid at position 549 for each strain is indicated. (b) Variation in the extent of syncytia formation (mean number of nuclei per syncytium) induced by proteins from two domestic dog strains (<i>Dog94SE</i> and <i>A75/17</i>), two non-dog strains (<i>5804P</i> and <i>Lion94SNP</i>) and one CDV-H protein mutated at position 549 (<i>A75/17-549H</i>) in domestic dog (black bars), African lion (grey bars) or domestic cat SLAM-expressing cells (white bars). Error bars indicate standard deviations of six independent experiments. (c) Appearance of syncytia upon expression of CDV-H and CDV-F proteins from two dog strains (<i>Dog94SE</i> and <i>A75/17</i>), two non-dog strains (<i>5804P</i> & <i>Lion94SNP</i>) and one mutated CDV-H protein coding 549H (<i>A75/17-549H</i>) in domestic dog SLAM, African lion SLAM and domestic cat SLAM cells. Photos were taken 12 hours post transfection at 100× magnification.</p>", "links"=>[], "tags"=>["cdv-h", "cdv", "strains", "interactions", "carnivore"], "article_id"=>197881, "categories"=>["Virology", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Veljko M. Nikolin", "Klaus Osterrieder", "Veronika von Messling", "Heribert Hofer", "Danielle Anderson", "Edward Dubovi", "Edgar Brunner", "Marion L. East"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0050955.g002", "stats"=>{"downloads"=>2, "page_views"=>55, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_the_CDV_H_protein_from_CDV_strains_and_their_interactions_with_carnivore_SLAM_receptors_/197881", "title"=>"Characterization of the CDV-H protein from CDV strains and their interactions with carnivore SLAM receptors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-11 02:11:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/527613"], "description"=>"<p>Predictions designed for CDV-H proteins were tested in an <i>in vitro</i> fusion assay (FA) and for CDV strains tested in an <i>in vitro</i> virus titration assay (TA). Strong co-evolution of CDV in a homogeneous environment (domestic dog) should produce strains that express specialist traits. Weak co-evolution of CDV in heterogeneous environments (non-dog carnivores) should produce strains expressing generalist traits. The homogeneous experimental environment is Vero cells expressing domestic dog SLAM. The heterogeneous experimental environment is Vero cells expressing African lion SLAM. The last two columns summarize the experimental results from this study.</p>", "links"=>[], "tags"=>["generalist", "canine", "distemper", "strains", "receptors"], "article_id"=>198102, "categories"=>["Virology", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Veljko M. Nikolin", "Klaus Osterrieder", "Veronika von Messling", "Heribert Hofer", "Danielle Anderson", "Edward Dubovi", "Edgar Brunner", "Marion L. East"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0050955.t001", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predicted_expression_of_specialist_and_generalist_traits_by_canine_distemper_virus_strains_in_relation_to_different_host_species_receptors_SLAM_CD150_/198102", "title"=>"Predicted expression of specialist and generalist traits by canine distemper virus strains in relation to different host species receptors (SLAM CD150).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-12-11 02:15:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/285232", "https://ndownloader.figshare.com/files/285335", "https://ndownloader.figshare.com/files/285427", "https://ndownloader.figshare.com/files/285484", "https://ndownloader.figshare.com/files/285545", "https://ndownloader.figshare.com/files/285611"], "description"=>"<div><p>Theoretically, homogeneous environments favor the evolution of specialists whereas heterogeneous environments favor generalists. Canine distemper is a multi-host carnivore disease caused by canine distemper virus (CDV). The described cell receptor of CDV is SLAM (CD150). Attachment of CDV hemagglutinin protein (CDV-H) to this receptor facilitates fusion and virus entry in cooperation with the fusion protein (CDV-F). We investigated whether CDV strains co-evolved in the large, homogeneous domestic dog population exhibited specialist traits, and strains adapted to the heterogeneous environment of smaller populations of different carnivores exhibited generalist traits. Comparison of amino acid sequences of the SLAM binding region revealed higher similarity between sequences from Canidae species than to sequences from other carnivore families. Using an <em>in vitro</em> assay, we quantified syncytia formation mediated by CDV-H proteins from dog and non-dog CDV strains in cells expressing dog, lion or cat SLAM. CDV-H proteins from dog strains produced significantly higher values with cells expressing dog SLAM than with cells expressing lion or cat SLAM. CDV-H proteins from strains of non-dog species produced similar values in all three cell types, but lower values in cells expressing dog SLAM than the values obtained for CDV-H proteins from dog strains. By experimentally changing one amino acid (Y549H) in the CDV-H protein of one dog strain we decreased expression of specialist traits and increased expression of generalist traits, thereby confirming its functional importance. A virus titer assay demonstrated that dog strains produced higher titers in cells expressing dog SLAM than cells expressing SLAM of non-dog hosts, which suggested possible fitness benefits of specialization post-cell entry. We provide <em>in vitro</em> evidence for the expression of specialist and generalist traits by CDV strains, and fitness trade-offs across carnivore host environments caused by antagonistic pleiotropy. These findings extend knowledge on CDV molecular epidemiology of particular relevance to wild carnivores.</p> </div>", "links"=>[], "tags"=>["antagonistic", "pleiotropy", "trade-offs", "generalist", "traits", "strains", "canine", "distemper", "virus"], "article_id"=>116222, "categories"=>["Biological Sciences", "Cancer", "Microbiology", "Evolutionary Biology"], "users"=>["Veljko M. Nikolin", "Klaus Osterrieder", "Veronika von Messling", "Heribert Hofer", "Danielle Anderson", "Edward Dubovi", "Edgar Brunner", "Marion L. East"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0050955.s001", "https://dx.doi.org/10.1371/journal.pone.0050955.s002", "https://dx.doi.org/10.1371/journal.pone.0050955.s003", "https://dx.doi.org/10.1371/journal.pone.0050955.s004", "https://dx.doi.org/10.1371/journal.pone.0050955.s005", "https://dx.doi.org/10.1371/journal.pone.0050955.s006"], "stats"=>{"downloads"=>8, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Antagonistic_Pleiotropy_and_Fitness_Trade_Offs_Reveal_Specialist_and_Generalist_Traits_in_Strains_of_Canine_Distemper_Virus__/116222", "title"=>"Antagonistic Pleiotropy and Fitness Trade-Offs Reveal Specialist and Generalist Traits in Strains of Canine Distemper Virus", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-12-11 01:43:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/527520"], "description"=>"<p>Virus titers produced by domestic dog strains (a) <i>Dog94SE</i> and (b) <i>A75/17</i>, and non-dog CDV strains (c) <i>5804P</i> and (d) <i>Lion94SNP</i> after 60 h of growth on cells expressing SLAM receptors from different host species. Cells expressing domestic dog SLAM (black bars), African lion SLAM (grey bars), domestic cat SLAM (white bars) and Vero (SLAM negative) cells (hatched bars). Titers were determined using the limited dilution method and expressed as log<sub>10</sub> TCID<sub>50</sub>/ml. Values shown represent the mean of six independent experiments; error bars indicate standard deviations. (e) The syncytia produced by infection with four CDV strains used in this study on domestic dog, African lion and domestic cat SLAM-expressing cell lines. Photographs were taken 40 h after infection using phase contrast at 100× magnification.</p>", "links"=>[], "tags"=>["titers", "syncytia", "produced", "vero", "cells", "expressing", "receptors", "hosts", "infected", "non-dog", "cdv", "strains"], "article_id"=>197993, "categories"=>["Virology", "Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Veljko M. Nikolin", "Klaus Osterrieder", "Veronika von Messling", "Heribert Hofer", "Danielle Anderson", "Edward Dubovi", "Edgar Brunner", "Marion L. East"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0050955.g003", "stats"=>{"downloads"=>2, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Virus_titers_and_syncytia_formation_produced_by_parental_Vero_cells_and_Vero_cells_expressing_SLAM_receptors_of_different_hosts_infected_with_dog_Dog94SE_and_A75_17_and_non_dog_CDV_strains_5804P_and_Lion94SNP_/197993", "title"=>"Virus titers and syncytia formation produced by parental Vero cells and Vero cells expressing SLAM receptors of different hosts infected with dog (<i>Dog94SE</i> and <i>A75/17</i>) and non-dog CDV strains (<i>5804P</i> and <i>Lion94SNP</i>).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-12-11 02:13:13"}

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Relative Metric

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