Independent repeated mutations within the alphaviruses Ross River virus and Barmah Forest virus indicates convergent evolution and past positive selection in ancestral populations despite ongoing purifying selection

Ross River virus (RRV) and Barmah Forest virus (BFV) are arthritogenic arthropod-borne viruses (arboviruses) that exhibit generalist host associations and share distributions in Australia and Papua New Guinea (PNG). Using stochastic mapping and discrete-trait phylogenetic analyses, we profiled the i...

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Main Authors: Pyke, AT, Wilson, DJ, Michie, A, Mackenzie, JS, Imrie, A, Cameron, J, Doggett, SL, Haniotis, J, Herrero, LJ, Caly, L, Lynch, SE, Mee, PT, Madzokere, ET, Ramirez, AL, Paramitha, D, Hobson-Peters, J, Smith, DW, Weir, R, Sullivan, M, Druce, J, Melville, L, Robson, J, Gibb, R, van den Hurk, AF
Format: Journal article
Language:English
Published: Oxford University Press 2024
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author Pyke, AT
Wilson, DJ
Michie, A
Mackenzie, JS
Imrie, A
Cameron, J
Doggett, SL
Haniotis, J
Herrero, LJ
Caly, L
Lynch, SE
Mee, PT
Madzokere, ET
Ramirez, AL
Paramitha, D
Hobson-Peters, J
Smith, DW
Weir, R
Sullivan, M
Druce, J
Melville, L
Robson, J
Gibb, R
van den Hurk, AF
author_facet Pyke, AT
Wilson, DJ
Michie, A
Mackenzie, JS
Imrie, A
Cameron, J
Doggett, SL
Haniotis, J
Herrero, LJ
Caly, L
Lynch, SE
Mee, PT
Madzokere, ET
Ramirez, AL
Paramitha, D
Hobson-Peters, J
Smith, DW
Weir, R
Sullivan, M
Druce, J
Melville, L
Robson, J
Gibb, R
van den Hurk, AF
author_sort Pyke, AT
collection OXFORD
description Ross River virus (RRV) and Barmah Forest virus (BFV) are arthritogenic arthropod-borne viruses (arboviruses) that exhibit generalist host associations and share distributions in Australia and Papua New Guinea (PNG). Using stochastic mapping and discrete-trait phylogenetic analyses, we profiled the independent evolution of RRV and BFV signature mutations. Analysis of 186 RRV and 88 BFV genomes demonstrated their viral evolution trajectories have involved repeated selection of mutations, particularly in the nonstructural protein 1 (nsP1) and envelope 3 (E3) genes suggesting convergent evolution. Convergent mutations in the nsP1 genes of RRV (residues 248 and 441) and BFV (residues 297 and 447) may be involved with catalytic enzyme mechanisms and host membrane interactions during viral RNA replication and capping. Convergent E3 mutations (RRV site 59 and BFV site 57) may be associated with enzymatic furin activity and cleavage of E3 from protein precursors assisting viral maturation and infectivity. Given their requirement to replicate in disparate insect and vertebrate hosts, convergent evolution in RRV and BFV may represent a dynamic link between their requirement to selectively ‘fine-tune’ intracellular host interactions and viral replicative enzymatic processes. Despite evidence of evolutionary convergence, selection pressure analyses did not reveal any RRV or BFV amino acid sites under strong positive selection and only weak positive selection for nonstructural protein sites. These findings may indicate that their alphavirus ancestors were subject to positive selection events which predisposed ongoing pervasive convergent evolution, and this largely supports continued purifying selection in RRV and BFV populations during their replication in mosquito and vertebrate hosts.
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spelling oxford-uuid:cfeb02c8-3926-4a68-bce7-2b8938b76b1b2024-10-29T20:03:41ZIndependent repeated mutations within the alphaviruses Ross River virus and Barmah Forest virus indicates convergent evolution and past positive selection in ancestral populations despite ongoing purifying selectionJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:cfeb02c8-3926-4a68-bce7-2b8938b76b1bEnglishJisc Publications RouterOxford University Press2024Pyke, ATWilson, DJMichie, AMackenzie, JSImrie, ACameron, JDoggett, SLHaniotis, JHerrero, LJCaly, LLynch, SEMee, PTMadzokere, ETRamirez, ALParamitha, DHobson-Peters, JSmith, DWWeir, RSullivan, MDruce, JMelville, LRobson, JGibb, Rvan den Hurk, AFRoss River virus (RRV) and Barmah Forest virus (BFV) are arthritogenic arthropod-borne viruses (arboviruses) that exhibit generalist host associations and share distributions in Australia and Papua New Guinea (PNG). Using stochastic mapping and discrete-trait phylogenetic analyses, we profiled the independent evolution of RRV and BFV signature mutations. Analysis of 186 RRV and 88 BFV genomes demonstrated their viral evolution trajectories have involved repeated selection of mutations, particularly in the nonstructural protein 1 (nsP1) and envelope 3 (E3) genes suggesting convergent evolution. Convergent mutations in the nsP1 genes of RRV (residues 248 and 441) and BFV (residues 297 and 447) may be involved with catalytic enzyme mechanisms and host membrane interactions during viral RNA replication and capping. Convergent E3 mutations (RRV site 59 and BFV site 57) may be associated with enzymatic furin activity and cleavage of E3 from protein precursors assisting viral maturation and infectivity. Given their requirement to replicate in disparate insect and vertebrate hosts, convergent evolution in RRV and BFV may represent a dynamic link between their requirement to selectively ‘fine-tune’ intracellular host interactions and viral replicative enzymatic processes. Despite evidence of evolutionary convergence, selection pressure analyses did not reveal any RRV or BFV amino acid sites under strong positive selection and only weak positive selection for nonstructural protein sites. These findings may indicate that their alphavirus ancestors were subject to positive selection events which predisposed ongoing pervasive convergent evolution, and this largely supports continued purifying selection in RRV and BFV populations during their replication in mosquito and vertebrate hosts.
spellingShingle Pyke, AT
Wilson, DJ
Michie, A
Mackenzie, JS
Imrie, A
Cameron, J
Doggett, SL
Haniotis, J
Herrero, LJ
Caly, L
Lynch, SE
Mee, PT
Madzokere, ET
Ramirez, AL
Paramitha, D
Hobson-Peters, J
Smith, DW
Weir, R
Sullivan, M
Druce, J
Melville, L
Robson, J
Gibb, R
van den Hurk, AF
Independent repeated mutations within the alphaviruses Ross River virus and Barmah Forest virus indicates convergent evolution and past positive selection in ancestral populations despite ongoing purifying selection
title Independent repeated mutations within the alphaviruses Ross River virus and Barmah Forest virus indicates convergent evolution and past positive selection in ancestral populations despite ongoing purifying selection
title_full Independent repeated mutations within the alphaviruses Ross River virus and Barmah Forest virus indicates convergent evolution and past positive selection in ancestral populations despite ongoing purifying selection
title_fullStr Independent repeated mutations within the alphaviruses Ross River virus and Barmah Forest virus indicates convergent evolution and past positive selection in ancestral populations despite ongoing purifying selection
title_full_unstemmed Independent repeated mutations within the alphaviruses Ross River virus and Barmah Forest virus indicates convergent evolution and past positive selection in ancestral populations despite ongoing purifying selection
title_short Independent repeated mutations within the alphaviruses Ross River virus and Barmah Forest virus indicates convergent evolution and past positive selection in ancestral populations despite ongoing purifying selection
title_sort independent repeated mutations within the alphaviruses ross river virus and barmah forest virus indicates convergent evolution and past positive selection in ancestral populations despite ongoing purifying selection
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