A transmission-virulence evolutionary trade-off explains attenuation of HIV-1 in Uganda

Evolutionary theory hypothesizes that intermediate virulence maximizes pathogen fitness as a result of a trade-off between virulence and transmission, but empirical evidence remains scarce. We bridge this gap using data from a large and long-standing HIV-1 prospective cohort, in Uganda. We use an ep...

Full description

Saved in:
Bibliographic Details
Published ineLife Vol. 5
Main Authors Blanquart, François, Grabowski, Mary Kate, Herbeck, Joshua, Nalugoda, Fred, Serwadda, David, Eller, Michael A, Robb, Merlin L, Gray, Ronald, Kigozi, Godfrey, Laeyendecker, Oliver, Lythgoe, Katrina A, Nakigozi, Gertrude, Quinn, Thomas C, Reynolds, Steven J, Wawer, Maria J, Fraser, Christophe
Format Journal Article
LanguageEnglish
Published England eLife Science Publications, Ltd 05.11.2016
eLife Sciences Publications Ltd
eLife Sciences Publications, Ltd
Subjects
Acquired immune deficiency syndrome
adaptation
AIDS
Asymptomatic infection
Biological Evolution
Epidemiology
Epidemiology and Global Health
Evolution
Generalized linear models
Genetic Fitness - genetics
Genomics and Evolutionary Biology
Health aspects
Health sciences
HIV
HIV Infections - epidemiology
HIV Infections - genetics
HIV Infections - virology
HIV-1 - classification
HIV-1 - genetics
HIV-1 - pathogenicity
Host-Pathogen Interactions - genetics
Human immunodeficiency virus
Humans
Hypotheses
Infections
Infectious diseases
Models, Biological
Observations
Pathogens
Public health
quantitative genetics
Reproductive fitness
selection
transmission-virulence trade-off
Trends
Uganda - epidemiology
viral evolution
Viral Load - genetics
Virulence
Virulence (Microbiology)
Uganda
global health
epidemiology
quantitative genetics
evolutionary biology
selection
viral evolution
adaptation
genomics
virus
transmission-virulence trade-off
Online AccessGet full text
ISSN2050-084X
2050-084X
DOI10.7554/eLife.20492

Cover

Abstract Evolutionary theory hypothesizes that intermediate virulence maximizes pathogen fitness as a result of a trade-off between virulence and transmission, but empirical evidence remains scarce. We bridge this gap using data from a large and long-standing HIV-1 prospective cohort, in Uganda. We use an epidemiological-evolutionary model parameterised with this data to derive evolutionary predictions based on analysis and detailed individual-based simulations. We robustly predict stabilising selection towards a low level of virulence, and rapid attenuation of the virus. Accordingly, set-point viral load, the most common measure of virulence, has declined in the last 20 years. Our model also predicts that subtype A is slowly outcompeting subtype D, with both subtypes becoming less virulent, as observed in the data. Reduction of set-point viral loads should have resulted in a 20% reduction in incidence, and a three years extension of untreated asymptomatic infection, increasing opportunities for timely treatment of infected individuals.
AbstractList Evolutionary theory hypothesizes that intermediate virulence maximizes pathogen fitness as a result of a trade-off between virulence and transmission, but empirical evidence remains scarce. We bridge this gap using data from a large and long-standing HIV-1 prospective cohort, in Uganda. We use an epidemiological-evolutionary model parameterised with this data to derive evolutionary predictions based on analysis and detailed individual-based simulations. We robustly predict stabilising selection towards a low level of virulence, and rapid attenuation of the virus. Accordingly, set-point viral load, the most common measure of virulence, has declined in the last 20 years. Our model also predicts that subtype A is slowly outcompeting subtype D, with both subtypes becoming less virulent, as observed in the data. Reduction of set-point viral loads should have resulted in a 20% reduction in incidence, and a three years extension of untreated asymptomatic infection, increasing opportunities for timely treatment of infected individuals.
Evolutionary theory hypothesizes that intermediate virulence maximizes pathogen fitness as a result of a trade-off between virulence and transmission, but empirical evidence remains scarce. We bridge this gap using data from a large and long-standing HIV-1 prospective cohort, in Uganda. We use an epidemiological-evolutionary model parameterised with this data to derive evolutionary predictions based on analysis and detailed individual-based simulations. We robustly predict stabilising selection towards a low level of virulence, and rapid attenuation of the virus. Accordingly, set-point viral load, the most common measure of virulence, has declined in the last 20 years. Our model also predicts that subtype A is slowly outcompeting subtype D, with both subtypes becoming less virulent, as observed in the data. Reduction of set-point viral loads should have resulted in a 20% reduction in incidence, and a three years extension of untreated asymptomatic infection, increasing opportunities for timely treatment of infected individuals. DOI:
Evolutionary theory hypothesizes that intermediate virulence maximizes pathogen fitness as a result of a trade-off between virulence and transmission, but empirical evidence remains scarce. We bridge this gap using data from a large and long-standing HIV-1 prospective cohort, in Uganda. We use an epidemiological-evolutionary model parameterised with this data to derive evolutionary predictions based on analysis and detailed individual-based simulations. We robustly predict stabilising selection towards a low level of virulence, and rapid attenuation of the virus. Accordingly, set-point viral load, the most common measure of virulence, has declined in the last 20 years. Our model also predicts that subtype A is slowly outcompeting subtype D, with both subtypes becoming less virulent, as observed in the data. Reduction of set-point viral loads should have resulted in a 20% reduction in incidence, and a three years extension of untreated asymptomatic infection, increasing opportunities for timely treatment of infected individuals.DOI: http://dx.doi.org/10.7554/eLife.20492.001
Evolutionary theory hypothesizes that intermediate virulence maximizes pathogen fitness as a result of a trade-off between virulence and transmission, but empirical evidence remains scarce. We bridge this gap using data from a large and long-standing HIV-1 prospective cohort, in Uganda. We use an epidemiological-evolutionary model parameterised with this data to derive evolutionary predictions based on analysis and detailed individual-based simulations. We robustly predict stabilising selection towards a low level of virulence, and rapid attenuation of the virus. Accordingly, set-point viral load, the most common measure of virulence, has declined in the last 20 years. Our model also predicts that subtype A is slowly outcompeting subtype D, with both subtypes becoming less virulent, as observed in the data. Reduction of set-point viral loads should have resulted in a 20% reduction in incidence, and a three years extension of untreated asymptomatic infection, increasing opportunities for timely treatment of infected individuals. DOI: http://dx.doi.org/10.7554/eLife.20492.001
Audience Academic
Author Grabowski, Mary Kate
Robb, Merlin L
Blanquart, François
Serwadda, David
Kigozi, Godfrey
Lythgoe, Katrina A
Quinn, Thomas C
Nalugoda, Fred
Eller, Michael A
Laeyendecker, Oliver
Reynolds, Steven J
Herbeck, Joshua
Fraser, Christophe
Gray, Ronald
Nakigozi, Gertrude
Wawer, Maria J
Author_xml – sequence: 1
  givenname: François
  orcidid: 0000-0003-0591-2466
  surname: Blanquart
  fullname: Blanquart, François
  organization: MRC Centre for Outbreak Analysis and Modelling, Imperial College London, London, United Kingdom, Department of Infectious Disease Epidemiology, Imperial College London, London, United Kingdom, School of Public Health, Imperial College London, London, United Kingdom
– sequence: 2
  givenname: Mary Kate
  surname: Grabowski
  fullname: Grabowski, Mary Kate
  organization: Department of Epidemiology, Johns Hopkins University, Baltimore, United States, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, United States
– sequence: 3
  givenname: Joshua
  orcidid: 0000-0003-4577-7406
  surname: Herbeck
  fullname: Herbeck, Joshua
  organization: International Clinical Research Center, University of Washington, Seattle, United States, Department of Global Health, University of Washington, Seattle, United States
– sequence: 4
  givenname: Fred
  surname: Nalugoda
  fullname: Nalugoda, Fred
  organization: Rakai Health Sciences Program, Entebbe, Uganda
– sequence: 5
  givenname: David
  surname: Serwadda
  fullname: Serwadda, David
  organization: Rakai Health Sciences Program, Entebbe, Uganda, School of Public Health, Makerere University, Kampala, Uganda
– sequence: 6
  givenname: Michael A
  surname: Eller
  fullname: Eller, Michael A
  organization: U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, United States, Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, United States
– sequence: 7
  givenname: Merlin L
  surname: Robb
  fullname: Robb, Merlin L
  organization: U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, United States, Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, United States
– sequence: 8
  givenname: Ronald
  surname: Gray
  fullname: Gray, Ronald
  organization: Department of Epidemiology, Johns Hopkins University, Baltimore, United States, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, United States, Rakai Health Sciences Program, Entebbe, Uganda
– sequence: 9
  givenname: Godfrey
  surname: Kigozi
  fullname: Kigozi, Godfrey
  organization: Rakai Health Sciences Program, Entebbe, Uganda
– sequence: 10
  givenname: Oliver
  surname: Laeyendecker
  fullname: Laeyendecker, Oliver
  organization: Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, United States, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, United States
– sequence: 11
  givenname: Katrina A
  surname: Lythgoe
  fullname: Lythgoe, Katrina A
  organization: MRC Centre for Outbreak Analysis and Modelling, Imperial College London, London, United Kingdom, Department of Infectious Disease Epidemiology, Imperial College London, London, United Kingdom, School of Public Health, Imperial College London, London, United Kingdom, Department of Zoology, University of Oxford, Oxford, United Kingdom
– sequence: 12
  givenname: Gertrude
  surname: Nakigozi
  fullname: Nakigozi, Gertrude
  organization: Rakai Health Sciences Program, Entebbe, Uganda
– sequence: 13
  givenname: Thomas C
  surname: Quinn
  fullname: Quinn, Thomas C
  organization: Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, United States, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, United States
– sequence: 14
  givenname: Steven J
  surname: Reynolds
  fullname: Reynolds, Steven J
  organization: Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, United States, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, United States
– sequence: 15
  givenname: Maria J
  surname: Wawer
  fullname: Wawer, Maria J
  organization: Department of Epidemiology, Johns Hopkins University, Baltimore, United States, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, United States
– sequence: 16
  givenname: Christophe
  surname: Fraser
  fullname: Fraser, Christophe
  organization: MRC Centre for Outbreak Analysis and Modelling, Imperial College London, London, United Kingdom, Department of Infectious Disease Epidemiology, Imperial College London, London, United Kingdom, School of Public Health, Imperial College London, London, United Kingdom, Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
BackLink https://www.ncbi.nlm.nih.gov/pubmed/27815945$$D View this record in MEDLINE/PubMed
BookMark eNptkk1vEzEQhi1UREvoiTtaiQsIbfDneveCFFVAI0VCAgrcLK89Do42drrejcq_x0laaKraB4_Gz7wej97n6CTEAAi9JHgqheDvYeEdTCnmDX2CzigWuMQ1_3VyLz5F5ymtcF6S1zVpnqFTKmsiGi7O0M9ZMfQ6pLVPycdQbn0_dhAMFLCN3TjknO7_7BgLZXSugJtNp31IhR4GCKPeEUV0xeX8R0kKH4qrpQ5Wv0BPne4SnN-eE3T16eP3i8ty8eXz_GK2KI2Q1VA2jWitlpQ6DK3A0jRQO0mx0W0lCbaYtRxjSi0RtdGc0RosFyAZryvmLGMTND_o2qhXatP7dW5XRe3VPhH7pdL94E0Hqm1aSzRjvNGGW6ZrXQnHMCXCUVfncII-HLQ2Y7sGayDkb3dHosc3wf9Wy7hVguT2JM0Cb24F-ng9QhpUHquBrtMB4pgUqVklmeRcZPT1A3QVxz7kUSnSCMYIw438Ty11_oAPLuZ3zU5UzbjEFa0quaOmj1B5W1h7k_3ifM4fFbw9KsjMADfDUo8pqfm3r8fsq_tD-TeNOwtlgBwA08eUenDK-GFvi9yF7xTBaudUtXeq2js117x7UHMn-xj9F0N753I
CitedBy_id crossref_primary_10_1111_eva_13310
crossref_primary_10_1002_ece3_8673
crossref_primary_10_1371_journal_pcbi_1005228
crossref_primary_10_1016_j_hlife_2024_03_006
crossref_primary_10_3389_fviro_2024_1379217
crossref_primary_10_1111_jeb_14053
crossref_primary_10_1007_s42977_023_00159_2
crossref_primary_10_1098_rspb_2023_2043
crossref_primary_10_1038_s41598_022_18507_y
crossref_primary_10_1371_journal_pcbi_1005453
crossref_primary_10_1038_s41576_018_0055_5
crossref_primary_10_1371_journal_pgen_1007718
crossref_primary_10_1038_s41579_018_0120_2
crossref_primary_10_1098_rsos_181577
crossref_primary_10_1126_science_abn4887
crossref_primary_10_1038_s41467_018_04595_w
crossref_primary_10_1111_ele_14218
crossref_primary_10_1111_eva_12458
crossref_primary_10_1371_journal_ppat_1007167
crossref_primary_10_1089_aid_2020_0062
crossref_primary_10_1371_journal_pntd_0011340
crossref_primary_10_3390_v14020187
crossref_primary_10_1093_ve_veab011
crossref_primary_10_1016_j_jtbi_2021_110900
crossref_primary_10_1093_ve_vey032
crossref_primary_10_7717_peerj_9578
crossref_primary_10_3390_ani12010002
crossref_primary_10_1126_science_abk1688
crossref_primary_10_1089_aid_2019_0150
crossref_primary_10_1371_journal_pmed_1002468
crossref_primary_10_1111_evo_13840
crossref_primary_10_1186_s12931_020_01551_5
crossref_primary_10_1186_s12977_021_00554_4
crossref_primary_10_1016_j_mib_2022_01_009
crossref_primary_10_1093_ve_vey015
crossref_primary_10_1016_j_mam_2022_101159
Cites_doi 10.1093/ve/vew028
10.1101/058503
10.7554/eLife.11282
10.1016/j.cub.2009.11.055
10.1098/rsif.2015.0888
10.1017/S0031182000055360
10.1371/journal.pcbi.1003673
10.1093/jn/135.4.938
10.1086/379333
10.1016/j.micinf.2008.01.013
10.1016/S1473-3099(12)70037-3
10.1371/journal.pcbi.1002185
10.1099/vir.0.000107
10.1086/527416
10.1073/pnas.1413339111
10.1126/science.1093166
10.1017/S003118201500092X
10.2307/2640710
10.1126/science.1101786
10.1097/QAD.0b013e32834db418
10.1016/S0140-6736(06)68541-3
10.1001/jama.2013.280923
10.1073/pnas.0708559104
10.1126/science.1254031
10.1098/rsif.2009.0384
10.1016/S0140-6736(05)17743-5
10.1089/aid.2010.0054
10.1046/j.1365-3156.2003.01176.x
10.1258/ijsa.2009.009067
10.1126/science.1243727
10.1016/j.tim.2016.04.008
10.1079/PHN2005912
10.1086/425042
10.1371/journal.pmed.1001801
10.1111/j.1365-3156.2006.01740.x
10.1017/S0003356100037752
10.1111/j.1420-9101.2008.01658.x
10.1097/00002030-200010200-00021
10.1093/oxfordjournals.aje.a008981
10.1084/jem.20072457
10.1128/JVI.00580-08
10.1086/444543
10.1016/S0140-6736(98)06439-3
10.1371/journal.ppat.1003209
10.1371/journal.ppat.1000365
10.1097/00002030-200111090-00013
10.1016/S0140-6736(94)90133-3
10.1073/pnas.0710909105
10.2307/1943014
10.2307/2407703
10.1086/341249
10.7554/eLife.01123
10.1111/j.1558-5646.2011.01533.x
10.1371/journal.ppat.1000876
10.1371/journal.ppat.1002321
10.1097/QAD.0b013e328330cc08
10.1086/382548
10.1016/S1473-3099(10)70093-1
10.1016/S0140-6736(98)02372-1
10.1111/j.1461-0248.2007.01091.x
10.1086/590501
10.1016/S2352-3018(14)00002-2
10.1006/jtbi.1994.1146
10.1371/journal.ppat.1004112
10.1038/227520a0
ContentType Journal Article
Copyright COPYRIGHT 2016 eLife Science Publications, Ltd.
2016, Blanquart et al. This work is licensed under the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/3.0/ ) (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2016, Blanquart et al 2016 Blanquart et al
Copyright_xml – notice: COPYRIGHT 2016 eLife Science Publications, Ltd.
– notice: 2016, Blanquart et al. This work is licensed under the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/3.0/ ) (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2016, Blanquart et al 2016 Blanquart et al
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
ISR
3V.
7X7
7XB
88E
88I
8FE
8FH
8FI
8FJ
8FK
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
FYUFA
GHDGH
GNUQQ
HCIFZ
K9.
LK8
M0S
M1P
M2P
M7P
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
Q9U
7X8
5PM
DOA
DOI 10.7554/eLife.20492
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Gale In Context: Science
ProQuest Central (Corporate)
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
Science Database (Alumni Edition)
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Collection
ProQuest Central Database Suite (ProQuest)
Natural Science Collection
ProQuest One
ProQuest Central
Proquest Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
SciTech Collection (ProQuest)
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
ProQuest Health & Medical Collection
Medical Database
Science Database
Biological Science Database (ProQuest)
ProQuest Central Premium
ProQuest One Academic (New)
ProQuest Publicly Available Content Database
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
ProQuest Central Basic
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Publicly Available Content Database
ProQuest Central Student
ProQuest One Academic Middle East (New)
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
ProQuest Central China
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest Health & Medical Research Collection
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Health & Medical Research Collection
Biological Science Collection
ProQuest Central (New)
ProQuest Medical Library (Alumni)
ProQuest Science Journals (Alumni Edition)
ProQuest Biological Science Collection
ProQuest Central Basic
ProQuest Science Journals
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
ProQuest Hospital Collection (Alumni)
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
ProQuest One Academic
ProQuest One Academic (New)
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList
MEDLINE
CrossRef

MEDLINE - Academic
Publicly Available Content Database
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 4
  dbid: BENPR
  name: ProQuest Central Database Suite (ProQuest)
  url: http://www.proquest.com/pqcentral?accountid=15518
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
Public Health
EISSN 2050-084X
ExternalDocumentID oai_doaj_org_article_b9bd1a3349ac4d3a8a65f30215f2f85f
PMC5115872
A470626677
27815945
10_7554_eLife_20492
Genre Research Support, U.S. Gov't, Non-P.H.S
Research Support, Non-U.S. Gov't
Journal Article
Research Support, N.I.H., Extramural
GeographicLocations Uganda
GeographicLocations_xml – name: Uganda
GrantInformation_xml – fundername: FIC NIH HHS
  grantid: D43 TW000010
– fundername: European Research Council
  grantid: 339251
– fundername: NIAID NIH HHS
  grantid: K01 AI125086
– fundername: NIAID NIH HHS
  grantid: R01 AI108490
– fundername: NIAID NIH HHS
  grantid: P30 AI027757
– fundername: ;
  grantid: R01 AI29314
– fundername: ;
– fundername: ;
  grantid: U01 AI11171-01-02
– fundername: ;
  grantid: P30AI027757
– fundername: ;
  grantid: R01AI108490
– fundername: ;
  grantid: 5P30 HD 06268
– fundername: ;
  grantid: Intra European Fellowship 657768
– fundername: ;
  grantid: 5024-30
– fundername: ;
  grantid: PBDR-339251
– fundername: ;
  grantid: 5D43TW00010
GroupedDBID 53G
5VS
7X7
88E
88I
8FE
8FH
8FI
8FJ
AAFWJ
AAKDD
AAYXX
ABUWG
ACGFO
ACGOD
ACPRK
ADBBV
ADRAZ
AENEX
AFKRA
AFPKN
ALIPV
ALMA_UNASSIGNED_HOLDINGS
AOIJS
AZQEC
BAWUL
BBNVY
BCNDV
BENPR
BHPHI
BPHCQ
BVXVI
CCPQU
CITATION
DIK
DWQXO
EMOBN
FYUFA
GNUQQ
GROUPED_DOAJ
GX1
H13
HCIFZ
HMCUK
HYE
IAO
IEA
IHR
INH
INR
ISR
ITC
KQ8
LK8
M1P
M2P
M48
M7P
M~E
NQS
OK1
PGMZT
PHGZM
PHGZT
PIMPY
PQQKQ
PROAC
PSQYO
RHI
RNS
RPM
UKHRP
CGR
CUY
CVF
ECM
EIF
NPM
PJZUB
PPXIY
PQGLB
PMFND
3V.
7XB
8FK
K9.
PKEHL
PQEST
PQUKI
PRINS
Q9U
7X8
PUEGO
5PM
ID FETCH-LOGICAL-c576t-995bda722f0eb507c9e8f720cab6710d03b40022d158ca4328ed45e734863fd33
IEDL.DBID M48
ISSN 2050-084X
IngestDate Wed Aug 27 01:29:04 EDT 2025
Thu Aug 21 18:21:34 EDT 2025
Fri Sep 05 02:51:09 EDT 2025
Fri Jul 25 09:48:38 EDT 2025
Tue Jun 17 21:17:54 EDT 2025
Tue Jun 10 20:44:54 EDT 2025
Fri Jun 27 04:58:46 EDT 2025
Mon Jul 21 06:01:40 EDT 2025
Thu Apr 24 23:00:31 EDT 2025
Tue Jul 01 01:11:41 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Keywords global health
epidemiology
quantitative genetics
evolutionary biology
selection
viral evolution
adaptation
genomics
virus
transmission-virulence trade-off
Language English
License http://creativecommons.org/licenses/by/4.0
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c576t-995bda722f0eb507c9e8f720cab6710d03b40022d158ca4328ed45e734863fd33
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
ORCID 0000-0003-4577-7406
0000-0003-0591-2466
OpenAccessLink https://www.proquest.com/docview/1953313097?pq-origsite=%requestingapplication%&accountid=15518
PMID 27815945
PQID 1953313097
PQPubID 2045579
ParticipantIDs doaj_primary_oai_doaj_org_article_b9bd1a3349ac4d3a8a65f30215f2f85f
pubmedcentral_primary_oai_pubmedcentral_nih_gov_5115872
proquest_miscellaneous_1836737445
proquest_journals_1953313097
gale_infotracmisc_A470626677
gale_infotracacademiconefile_A470626677
gale_incontextgauss_ISR_A470626677
pubmed_primary_27815945
crossref_citationtrail_10_7554_eLife_20492
crossref_primary_10_7554_eLife_20492
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2016-11-05
PublicationDateYYYYMMDD 2016-11-05
PublicationDate_xml – month: 11
  year: 2016
  text: 2016-11-05
  day: 05
PublicationDecade 2010
PublicationPlace England
PublicationPlace_xml – name: England
– name: Cambridge
PublicationTitle eLife
PublicationTitleAlternate Elife
PublicationYear 2016
Publisher eLife Science Publications, Ltd
eLife Sciences Publications Ltd
eLife Sciences Publications, Ltd
Publisher_xml – name: eLife Science Publications, Ltd
– name: eLife Sciences Publications Ltd
– name: eLife Sciences Publications, Ltd
References Modjarrad (bib47) 2005; 192
Bartha (bib4) 2013; 2
Brown (bib11) 2004; 190
Hollingsworth (bib32) 2008; 198
Paz-Bailey (bib51) 2013; 62
Kouyos (bib37) 2011; 7
Berngruber (bib7) 2013; 9
Payne (bib50) 2014; 111
Farzadegan (bib21) 1998; 352
Mermin (bib44) 2006; 367
Sewankambo (bib58) 2000; 14
Herbeck (bib29) 2014; 10
Fawzi (bib22) 2005; 135
Conroy (bib14) 2010; 26
Fraser (bib23) 2007; 104
Troyer (bib63) 2009; 5
Hodcroft (bib31) 2014; 10
Hollingsworth (bib33) 2010; 6
Lenski (bib40) 1994; 169
Wawer (bib64) 1999; 353
Matthews (bib43) 2008; 82
Pritchard (bib53) 2010; 20
Leventhal (bib41) 2016; 24
Baum (bib5) 2013; 310
Brankin AE (bib10) 2009; 20
Carlson (bib13) 2014; 345
Goepfert (bib27) 2008; 205
Price (bib52) 1970; 227
Robertson (bib56) 1966; 8
Modjarrad (bib46) 2010; 10
de Roode (bib19) 2008; 105
Day (bib16) 2007; 10
Serwadda (bib57) 2003; 188
Anderson (bib3) 1982; 85
Lande (bib39) 1976; 30
Herbeck (bib30) 2012; 26
Fraser (bib24) 2014; 343
Mackinnon (bib42) 1999; 53
Kiwanuka (bib35) 2009; 23
Zanini (bib67) 2015; 4
Bolker (bib8) 2010; 7
Herbeck (bib28) 2016; 2
Shirreff (bib59) 2011; 7
Carlson (bib12) 2008; 10
Mitov (bib45) 2016
Bellan (bib6) 2015; 12
Mulder (bib48) 1994; 343
Gandhi (bib26) 2002; 35
Steyn (bib60) 2006; 9
Alizon (bib2) 2009; 22
Day (bib17) 2012; 66
Pantazis (bib49) 2014; 1
Stoneburner (bib61) 1996; 144
Reynolds (bib54) 2012; 12
Ahmed (bib1) 2001; 15
Stoneburner (bib62) 2004; 304
Kiwanuka (bib36) 2008; 197
Dwyer (bib20) 1990; 60
Kublin (bib38) 2005; 365
Yebra (bib66) 2015; 96
Friis (bib25) 2006; 11
World Health Organization (bib65) 2015
Cressler (bib15) 2016; 143
Day (bib18) 2004; 163
Roberts (bib55) 2015; 12
Bonhoeffer (bib9) 2004; 306
Kabatereine (bib34) 2004; 9
References_xml – volume: 2
  start-page: vew028
  year: 2016
  ident: bib28
  article-title: Evolution of HIV virulence in response to widespread scale up of antiretroviral therapy: a modeling study
  publication-title: Virus Evolution
  doi: 10.1093/ve/vew028
– year: 2016
  ident: bib45
  article-title: The heritability of pathogen traits-definitions and estimators
  publication-title: bioRxiv
  doi: 10.1101/058503
– volume: 4
  start-page: e11282
  year: 2015
  ident: bib67
  article-title: Population genomics of intrapatient HIV-1 evolution
  publication-title: eLife
  doi: 10.7554/eLife.11282
– volume: 20
  start-page: R208
  year: 2010
  ident: bib53
  article-title: The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation
  publication-title: Current Biology
  doi: 10.1016/j.cub.2009.11.055
– volume: 12
  start-page: 20150888
  year: 2015
  ident: bib55
  article-title: The impact of antiretroviral therapy on population-level virulence evolution of HIV-1
  publication-title: Journal of the Royal Society Interface
  doi: 10.1098/rsif.2015.0888
– volume: 85
  start-page: 411
  year: 1982
  ident: bib3
  article-title: Coevolution of hosts and parasites
  publication-title: Parasitology
  doi: 10.1017/S0031182000055360
– volume: 10
  start-page: e1003673
  year: 2014
  ident: bib29
  article-title: An HIV epidemic model based on viral load dynamics: value in assessing empirical trends in HIV virulence and community viral load
  publication-title: PLoS Computational Biology
  doi: 10.1371/journal.pcbi.1003673
– volume: 135
  start-page: 938
  year: 2005
  ident: bib22
  article-title: Studies of vitamins and minerals and HIV transmission and disease progression
  publication-title: The Journal of Nutrition
  doi: 10.1093/jn/135.4.938
– volume: 188
  start-page: 1492
  year: 2003
  ident: bib57
  article-title: Human immunodeficiency virus acquisition associated with genital ulcer disease and herpes simplex virus type 2 infection: a nested case-control study in Rakai, Uganda
  publication-title: The Journal of Infectious Diseases
  doi: 10.1086/379333
– volume: 10
  start-page: 455
  year: 2008
  ident: bib12
  article-title: HIV evolution in response to HLA-restricted CTL selection pressures: a population-based perspective
  publication-title: Microbes and Infection
  doi: 10.1016/j.micinf.2008.01.013
– volume: 12
  start-page: 441
  year: 2012
  ident: bib54
  article-title: Effect of daily aciclovir on HIV disease progression in individuals in Rakai, Uganda, co-infected with HIV-1 and herpes simplex virus type 2: a randomised, double-blind placebo-controlled trial
  publication-title: The Lancet Infectious Diseases
  doi: 10.1016/S1473-3099(12)70037-3
– volume-title: Glocal tuberculosis report 2015
  year: 2015
  ident: bib65
– volume: 7
  start-page: e1002185
  year: 2011
  ident: bib59
  article-title: Transmission selects for HIV-1 strains of intermediate virulence: a modelling approach
  publication-title: PLoS Computational Biology
  doi: 10.1371/journal.pcbi.1002185
– volume: 96
  start-page: 1890
  year: 2015
  ident: bib66
  article-title: Analysis of the history and spread of HIV-1 in Uganda using phylodynamics
  publication-title: Journal of General Virology
  doi: 10.1099/vir.0.000107
– volume: 197
  start-page: 707
  year: 2008
  ident: bib36
  article-title: Effect of human immunodeficiency virus type 1 (HIV‐1) subtype on disease progression in persons from rakai, uganda, with incident HIV‐1 infection
  publication-title: The Journal of Infectious Diseases
  doi: 10.1086/527416
– volume: 111
  start-page: E5393
  year: 2014
  ident: bib50
  article-title: Impact of HLA-driven HIV adaptation on virulence in populations of high HIV seroprevalence
  publication-title: PNAS
  doi: 10.1073/pnas.1413339111
– volume: 304
  start-page: 714
  year: 2004
  ident: bib62
  article-title: Population-level HIV declines and behavioral risk avoidance in Uganda
  publication-title: Science
  doi: 10.1126/science.1093166
– volume: 143
  start-page: 915
  year: 2016
  ident: bib15
  article-title: The adaptive evolution of virulence: a review of theoretical predictions and empirical tests
  publication-title: Parasitology
  doi: 10.1017/S003118201500092X
– volume: 53
  start-page: 689
  year: 1999
  ident: bib42
  article-title: Genetic relationships between parasite virulence and transmission in the rodent malaria plasmodium chabaudi
  publication-title: Evolution
  doi: 10.2307/2640710
– volume: 306
  start-page: 1547
  year: 2004
  ident: bib9
  article-title: Evidence for positive epistasis in HIV-1
  publication-title: Science
  doi: 10.1126/science.1101786
– volume: 26
  start-page: 193
  year: 2012
  ident: bib30
  article-title: Is the virulence of HIV changing? A meta-analysis of trends in prognostic markers of HIV disease progression and transmission
  publication-title: AIDS
  doi: 10.1097/QAD.0b013e32834db418
– volume: 367
  start-page: 1256
  year: 2006
  ident: bib44
  article-title: Effect of co-trimoxazole prophylaxis, antiretroviral therapy, and insecticide-treated bednets on the frequency of malaria in HIV-1-infected adults in Uganda: a prospective cohort study
  publication-title: The Lancet
  doi: 10.1016/S0140-6736(06)68541-3
– volume: 310
  start-page: 2154
  year: 2013
  ident: bib5
  article-title: Effect of micronutrient supplementation on disease progression in asymptomatic, antiretroviral-naive, HIV-infected adults in Botswana: a randomized clinical trial
  publication-title: JAMA
  doi: 10.1001/jama.2013.280923
– volume: 104
  start-page: 17441
  year: 2007
  ident: bib23
  article-title: Variation in HIV-1 set-point viral load: Epidemiological analysis and an evolutionary hypothesis
  publication-title: PNAS
  doi: 10.1073/pnas.0708559104
– volume: 345
  start-page: 1254031
  year: 2014
  ident: bib13
  article-title: HIV transmission. Selection bias at the heterosexual HIV-1 transmission bottleneck
  publication-title: Science
  doi: 10.1126/science.1254031
– volume: 7
  start-page: 811
  year: 2010
  ident: bib8
  article-title: Transient virulence of emerging pathogens
  publication-title: Journal of the Royal Society Interface
  doi: 10.1098/rsif.2009.0384
– volume: 365
  start-page: 233
  year: 2005
  ident: bib38
  article-title: Effect of Plasmodium falciparum malaria on concentration of HIV-1-RNA in the blood of adults in rural Malawi: a prospective cohort study
  publication-title: The Lancet
  doi: 10.1016/S0140-6736(05)17743-5
– volume: 26
  start-page: 1087
  year: 2010
  ident: bib14
  article-title: Changes in the distribution of HIV type 1 subtypes D and A in rakai district, uganda between 1994 and 2002
  publication-title: AIDS Research and Human Retroviruses
  doi: 10.1089/aid.2010.0054
– volume: 9
  start-page: 372
  year: 2004
  ident: bib34
  article-title: Epidemiology and geography of Schistosoma mansoni in Uganda: implications for planning control
  publication-title: Tropical Medicine and International Health
  doi: 10.1046/j.1365-3156.2003.01176.x
– volume: 20
  start-page: 650
  year: 2009
  ident: bib10
  article-title: Aetiology of genital ulcer disease in female partners of male participants in a circumcision trial in Uganda
  publication-title: International Journal of STD & AIDS
  doi: 10.1258/ijsa.2009.009067
– volume: 343
  start-page: 1243727
  year: 2014
  ident: bib24
  article-title: Virulence and pathogenesis of HIV-1 infection: an evolutionary perspective
  publication-title: Science
  doi: 10.1126/science.1243727
– volume: 24
  start-page: 687
  year: 2016
  ident: bib41
  article-title: Potential pitfalls in estimating viral load heritability
  publication-title: Trends in Microbiology
  doi: 10.1016/j.tim.2016.04.008
– volume: 9
  start-page: 644
  year: 2006
  ident: bib60
  article-title: Food variety and dietary diversity scores in children: are they good indicators of dietary adequacy?
  publication-title: Public Health Nutrition
  doi: 10.1079/PHN2005912
– volume: 190
  start-page: 1869
  year: 2004
  ident: bib11
  article-title: Helminth infection is not associated with faster progression of HIV disease in coinfected adults in Uganda
  publication-title: The Journal of Infectious Diseases
  doi: 10.1086/425042
– volume: 12
  start-page: e1001801
  year: 2015
  ident: bib6
  article-title: Reassessment of HIV-1 acute phase infectivity: accounting for heterogeneity and study design with simulated cohorts
  publication-title: PLoS Medicine
  doi: 10.1371/journal.pmed.1001801
– volume: 11
  start-page: 1849
  year: 2006
  ident: bib25
  article-title: Micronutrient interventions and HIV infection: a review of current evidence
  publication-title: Tropical Medicine and International Health
  doi: 10.1111/j.1365-3156.2006.01740.x
– volume: 8
  start-page: 95
  year: 1966
  ident: bib56
  article-title: A mathematical model of the culling process in dairy cattle
  publication-title: Animal Production
  doi: 10.1017/S0003356100037752
– volume: 22
  start-page: 245
  year: 2009
  ident: bib2
  article-title: Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future
  publication-title: Journal of Evolutionary Biology
  doi: 10.1111/j.1420-9101.2008.01658.x
– volume: 14
  start-page: 2391
  year: 2000
  ident: bib58
  article-title: Mortality associated with HIV infection in rural Rakai District, Uganda
  publication-title: AIDS
  doi: 10.1097/00002030-200010200-00021
– volume: 144
  start-page: 682
  year: 1996
  ident: bib61
  article-title: Human immunodeficiency virus infection dynamics in east Africa deduced from surveillance data
  publication-title: American Journal of Epidemiology
  doi: 10.1093/oxfordjournals.aje.a008981
– volume: 62
  start-page: 958
  year: 2013
  ident: bib51
  article-title: HIV testing and risk behaviors among gay, bisexual, and other men who have sex with men - United States
  publication-title: MMWR. Morbidity and Mortality Weekly Report
– volume: 205
  start-page: 1009
  year: 2008
  ident: bib27
  article-title: Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients
  publication-title: The Journal of Experimental Medicine
  doi: 10.1084/jem.20072457
– volume: 82
  start-page: 8548
  year: 2008
  ident: bib43
  article-title: Central role of reverting mutations in HLA associations with human immunodeficiency virus set point
  publication-title: Journal of Virology
  doi: 10.1128/JVI.00580-08
– volume: 192
  start-page: 1277
  year: 2005
  ident: bib47
  article-title: Treatment of intestinal helminths does not reduce plasma concentrations of HIV-1 RNA in coinfected Zambian adults
  publication-title: The Journal of Infectious Diseases
  doi: 10.1086/444543
– volume: 353
  start-page: 525
  year: 1999
  ident: bib64
  article-title: Control of sexually transmitted diseases for AIDS prevention in Uganda: a randomised community trial
  publication-title: The Lancet
  doi: 10.1016/S0140-6736(98)06439-3
– volume: 9
  start-page: e1003209
  year: 2013
  ident: bib7
  article-title: Evolution of virulence in emerging epidemics
  publication-title: PLoS Pathogens
  doi: 10.1371/journal.ppat.1003209
– volume: 5
  start-page: e1000365
  year: 2009
  ident: bib63
  article-title: Variable fitness impact of HIV-1 escape mutations to cytotoxic T lymphocyte (CTL) response
  publication-title: PLoS Pathogens
  doi: 10.1371/journal.ppat.1000365
– volume: 15
  start-page: 2171
  year: 2001
  ident: bib1
  article-title: HIV incidence and sexually transmitted disease prevalence associated with condom use: a population study in Rakai, Uganda
  publication-title: AIDS
  doi: 10.1097/00002030-200111090-00013
– volume: 343
  start-page: 1021
  year: 1994
  ident: bib48
  article-title: Two-year HIV-1-associated mortality in a Ugandan rural population
  publication-title: The Lancet
  doi: 10.1016/S0140-6736(94)90133-3
– volume: 105
  start-page: 7489
  year: 2008
  ident: bib19
  article-title: Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite
  publication-title: PNAS
  doi: 10.1073/pnas.0710909105
– volume: 60
  start-page: 423
  year: 1990
  ident: bib20
  article-title: A simulation model of the population dynamics and evolution of myxomatosis
  publication-title: Ecological Monographs
  doi: 10.2307/1943014
– volume: 30
  start-page: 314
  year: 1976
  ident: bib39
  article-title: Natural selection and random genetic drift in phenotypic evolution
  publication-title: Evolution
  doi: 10.2307/2407703
– volume: 35
  start-page: 313
  year: 2002
  ident: bib26
  article-title: Does patient sex affect human immunodeficiency virus levels?
  publication-title: Clinical Infectious Diseases
  doi: 10.1086/341249
– volume: 2
  start-page: e01123
  year: 2013
  ident: bib4
  article-title: A genome-to-genome analysis of associations between human genetic variation, HIV-1 sequence diversity, and viral control
  publication-title: eLife
  doi: 10.7554/eLife.01123
– volume: 66
  start-page: 1582
  year: 2012
  ident: bib17
  article-title: The evolutionary epidemiology of multilocus drug resistance
  publication-title: Evolution
  doi: 10.1111/j.1558-5646.2011.01533.x
– volume: 6
  start-page: e1000876
  year: 2010
  ident: bib33
  article-title: HIV-1 transmitting couples have similar viral load set-points in Rakai, Uganda
  publication-title: PLoS Pathogens
  doi: 10.1371/journal.ppat.1000876
– volume: 7
  start-page: e1002321
  year: 2011
  ident: bib37
  article-title: Assessing predicted HIV-1 replicative capacity in a clinical setting
  publication-title: PLoS Pathogens
  doi: 10.1371/journal.ppat.1002321
– volume: 23
  start-page: 2479
  year: 2009
  ident: bib35
  article-title: HIV-1 subtypes and differences in heterosexual HIV transmission among HIV-discordant couples in rakai, uganda
  publication-title: AIDS
  doi: 10.1097/QAD.0b013e328330cc08
– volume: 163
  start-page: E40
  year: 2004
  ident: bib18
  article-title: A general theory for the evolutionary dynamics of virulence
  publication-title: The American Naturalist
  doi: 10.1086/382548
– volume: 10
  start-page: 455
  year: 2010
  ident: bib46
  article-title: Effect of treating co-infections on HIV-1 viral load: a systematic review
  publication-title: The Lancet Infectious Diseases
  doi: 10.1016/S1473-3099(10)70093-1
– volume: 352
  start-page: 1510
  year: 1998
  ident: bib21
  article-title: Sex differences in HIV-1 viral load and progression to AIDS
  publication-title: The Lancet
  doi: 10.1016/S0140-6736(98)02372-1
– volume: 10
  start-page: 876
  year: 2007
  ident: bib16
  article-title: Applying population-genetic models in theoretical evolutionary epidemiology
  publication-title: Ecology Letters
  doi: 10.1111/j.1461-0248.2007.01091.x
– volume: 198
  start-page: 687
  year: 2008
  ident: bib32
  article-title: HIV-1 transmission, by stage of infection
  publication-title: The Journal of Infectious Diseases
  doi: 10.1086/590501
– volume: 1
  start-page: e119
  year: 2014
  ident: bib49
  article-title: Temporal trends in prognostic markers of HIV-1 virulence and transmissibility: an observational cohort study
  publication-title: The Lancet HIV
  doi: 10.1016/S2352-3018(14)00002-2
– volume: 169
  start-page: 253
  year: 1994
  ident: bib40
  article-title: The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses
  publication-title: Journal of Theoretical Biology
  doi: 10.1006/jtbi.1994.1146
– volume: 10
  start-page: e1004112
  year: 2014
  ident: bib31
  article-title: The contribution of viral genotype to plasma viral set-point in HIV infection
  publication-title: PLoS Pathogens
  doi: 10.1371/journal.ppat.1004112
– volume: 227
  start-page: 520
  year: 1970
  ident: bib52
  article-title: Selection and covariance
  publication-title: Nature
  doi: 10.1038/227520a0
SSID ssj0000748819
Score 2.3510718
Snippet Evolutionary theory hypothesizes that intermediate virulence maximizes pathogen fitness as a result of a trade-off between virulence and transmission, but...
SourceID doaj
pubmedcentral
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
SubjectTerms Acquired immune deficiency syndrome
adaptation
AIDS
Asymptomatic infection
Biological Evolution
Epidemiology
Epidemiology and Global Health
Evolution
Generalized linear models
Genetic Fitness - genetics
Genomics and Evolutionary Biology
Health aspects
Health sciences
HIV
HIV Infections - epidemiology
HIV Infections - genetics
HIV Infections - virology
HIV-1 - classification
HIV-1 - genetics
HIV-1 - pathogenicity
Host-Pathogen Interactions - genetics
Human immunodeficiency virus
Humans
Hypotheses
Infections
Infectious diseases
Models, Biological
Observations
Pathogens
Public health
quantitative genetics
Reproductive fitness
selection
transmission-virulence trade-off
Trends
Uganda - epidemiology
viral evolution
Viral Load - genetics
Virulence
Virulence (Microbiology)
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1ba9VAEF6kIPgi3o22EqUgCKHJ3vfxKJZTUR_Uo31bdje7baAk5VyK_fedSdLDCQq--JqZwO5cdmaTmW8IOSypNzFVvFDes4KLoAsXGAW_ciVPUkcvsRv5y1c5X_BPp-J0Z9QX1oQN8MCD4I688XXlGOPGBV4zp50UiWGkSjRpkfD0LU25c5nqz2AFhlmZoSFPQcg8ip-bhLCY3NBJCOqR-v88j3cC0rRYcif6HD8g98e0MZ8Ny31I7sT2Ebk7DJK8fkx-zfI1Bh1QGn79Kq6a5abvJsrj1WhbbnmNPHUsupTy-PvywjXtKkd4zXaA-867lM9PfhZV3rT54gw_MTwhi-OPPz7Mi3FkQhHg4rAujBG-dorSVEYPqV4wUSdFy-C8hFyiLpnnGLbrSujgOKM61lxEhLiRLNWMPSV7bdfG5yTXwnMXIfxLJbkrwfVV4MxFIbnUtKYZeXcrRRtGPHEca3Fh4V6BIre9yG0v8owcbpkvBxiNv7O9R3VsWRD7un8AFmFHi7D_soiMvEFlWkS3aLF85sxtVit78v2bnXFVwg1OKpWRtyNT6mDVwY3dCLB3BMSacO5POEGTYUq-tRk7uv_K4r9JBtmBAfLrLRnfxJK2NnYb4NEMZwRxLjLybDCx7b6p0pBmIkVNjG8imCmlbc57cHBIoIVW9MX_kORLcg_yQ9m3Xop9srdebuIB5GBr_6p3txtFay9q
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: ProQuest Central Database Suite (ProQuest)
  dbid: BENPR
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1ta9RAEF5qiyCIaNUarRKlIAihuX3PB5GrtFxFD6lW-y3s63lQkvNeiv33ziS5s0Hxa3YCm8zszLOzO88QcpBTW4Q44JmylmVcOJ0ZxyisK5PzKHWwEquRP43l6Jx_uBAXW2S8roXBa5Vrn9g4al87zJEf4nEPA4dbqHeznxl2jcLT1XULDdO1VvBvG4qxW2QHXLIGu985Oh5_PttkXSBgaoiBbaGeglB6GD5OI9Jl8oL2QlPD4P-3n74RqPqXKG9EpZP75F4HJ9Nhq_8HZCtUu-R222DyepfcbbNyaVts9JB8H6ZLDE6gXMySZVfT-aqpOkrDVWeDZn6NMj5kdYxp-DW7NNNqkSINZ9XSgqd1TEen37JBOq3S8wmmIh6R85Pjr-9HWddaIXOwwVhmRSGsN4rSmAcLkNAVQUdFc2esBMzhc2Y5hnc_ENoZzqgOnouAVDiSRc_YY7Jd1VV4QlItLDcBYIJUkpscXIRynJkgJJeaepqQN-u_WrqOdxzbX1yWsP9AFZSNCspGBQk52AjPWrqNf4sdoXo2IsiR3Tyo55OyW3KlLawfGMZ4YRz3zGgjRWSIcSKNWsSEvELllsiCUeE1m4lZLRbl6ZezcshVDjs9qVRCXndCsYZZO9NVLcC3I3FWT3K_JwmadP3htQ2VnZtYlH-MOiEvN8P4Jl59q0K9AhnNsJcQ5yIhe63Jbb6bKg1wFEdUzxh7P6Y_Uk1_NCTiALSFVvTp_6f1jNwBhCib4kuxT7aX81V4DihsaV90S-s3CZ8yBA
  priority: 102
  providerName: ProQuest
Title A transmission-virulence evolutionary trade-off explains attenuation of HIV-1 in Uganda
URI https://www.ncbi.nlm.nih.gov/pubmed/27815945
https://www.proquest.com/docview/1953313097
https://www.proquest.com/docview/1836737445
https://pubmed.ncbi.nlm.nih.gov/PMC5115872
https://doaj.org/article/b9bd1a3349ac4d3a8a65f30215f2f85f
Volume 5
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwdV3db9MwELfGJiReEN8LjCqgSUhIGWn8mSfUoU0dYhMaFPZm2Y5dKlXJ6Me0_vfcJWnVwHiNz1F8Pvt-5_h-R8hhmtnchz5LpLU0YdypxDiawboyKQtCeSswG_n8QgxH7PMVv9oh62KcrQLnd4Z2WE9qNJse3f5efYQFD_j1SII3_OC_TAIyXrIc9uI9cEkCo7DzFufXW7IEO-3nTX7e332QD1gqcOuY0rTlnGoO_3936i1X1b1GueWXTh-Rhy2gjAeNBTwmO758Qu43JSZXT8nPQbxAdwTTiediyc1ktqzzjGJ_01qdma1QpvBJFULsb6-nZlLOYyTeLBsi8LgK8fDsR9KPJ2U8GuPhwzMyOj35_mmYtMUUEgchxSLJc24LI7MspN4CCHS5V0FmqTNWAMooUmoZOvSiz5UzjGbKF4x7JL8RNBSUPie7ZVX6fRIrbpnxAAyEFMyksClIx6jxXDChsiKLyPu1FrVrmcax4MVUQ8SB2te19nWt_YgcboSvG4KNu8WOcTo2IsiKXT-oZmPdLjJtc1v0DaUsN44V1CgjeKCIakIWFA8ReYuTqZH3osSLNWOznM_12bdLPWAyhdhOSBmRd61QqOCrnWnzFGDsSJXVkTzoSMJMum7z2mb02q41_rWkgBtyaH6zacaeeNmt9NUSZBTF6kGM8Yi8aExsM-61pUZEdoyvo5huSzn5VdOGA7TmSmYv__vOV-QBwEFRZ1ryA7K7mC39a4BcC9sj9-SV7JG945OLr5e9-uCiVy-xP4JXLFQ
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3bbtNAEF1VqRBICEG5GQosqAgJyaqz3psfKpRCq4SmESpN6ZtZ27shUmWHXAr5Ob6NGdsJtUC89TU7keydy5kd75whZCdgSWRdm_sqSUKfi1T7Jg0Z-JUJuJPaJhK7kY8HsjvkH8_F-Qb5teqFwWuVq5hYBuqsSLFGvoufe0IIuJF6N_nu49Qo_Lq6GqFh6tEK2V5JMVY3dhzZ5Q84ws32eh9A368ZOzw4fd_16ykDfgq59tyPIpFkRjHmAptAdpRGVjvFgtQkEuA3C8KEI9JlbaFTw0OmbcaFRVYYGboMC6IAAZuQdkS8RTb3DwafTtZVHgBoDZhbNQYqgO5d2x87pOfkEWtAYTkx4G9cuAKMzUubV1Dw8C65U6evtFPZ2z2yYfMtcqMaaLncIrerKiCtmpvuky8dOkcwBGPCqpx_OZ4uyi4nai9rmzfTJcpk1i-co_bn5MKM8xlF2s-8oiGnhaPd3pnfpuOcDkdY-nhAhteyyQ9JKy9y-5hQLRJuLKQlUkluAghJKuWhsUJyqVnGPPJ2tatxWvOc47iNixjOO6iCuFRBXKrAIztr4UlF7_FvsX1Uz1oEObnLH4rpKK5dPE6iJGubMOSRSXkWGm2kcCHmVI45LZxHXqFyY2TdyPFaz8gsZrO49_kk7nAVwMlSKuWRN7WQK-CpU1N3ScC7I1FXQ3K7IQmaTJvLKxuK67A0i_84kUderpfxn3jVLrfFAmR0iLOLOBceeVSZ3Pq9mdKQ_uKKahhjY2OaK_n4W0laDom90Io9-f9jvSA3u6fH_bjfGxw9JbcgO5Vl46fYJq35dGGfQQY4T57XbkbJ1-v27N_F5G3q
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1tb9MwELamTSAkhGC8BQYENISEFDW1Hdv5MKGOrWrZqKZBx74Fx7FLpSkpfRn0L_KruEvSsgjEt32tr1Lie3nOF99zhOyGNI2ta_NApikLeGRUoA2j4Fc65E4omwrsRv44EL0h_3AenW-QX6teGLxWuYqJZaDOCoM18hZ-7mEQcGPZcvW1iJOD7rvJ9wAnSOGX1tU4DV2PWcj2SrqxusnjyC5_wHFuttc_AN2_prR7-Pl9L6gnDgQG8u55EMdRmmlJqQttCpmSia1ykoZGpwKgOAtZyhH1snakjOaMKpvxyCJDjGAuw-IowMGWBJQEn9vaPxycnK4rPgDWCvC3ahKUAOMtezx2SNXJY9qAxXJ6wN8YcQUkmxc4ryBi9y65U6eyfqeyvXtkw-bb5EY13HK5TW5XFUG_anS6T750_DkCIxgWVuiCy_F0UXY8-faytn89XaJMZoPCOd_-nFzocT7zkQI0ryjJ_cL5vf5Z0PbHuT8cYRnkARleyyY_JJt5kdvHxFdRyrWFFEVIwXUI4UkazrSNBBeKZtQjb1e7mpia8xxHb1wkcPZBFSSlCpJSBR7ZXQtPKqqPf4vto3rWIsjPXf5QTEdJ7e5JGqdZWzPGY214xrTSInIM8ytHnYqcR16hchNk4MjRlkd6MZsl_U-nSYfLEE6ZQkqPvKmFXAFPbXTdMQHvjqRdDcmdhiRo0jSXVzaU1CFqlvxxKI-8XC_jP_HaXW6LBcgohnOMOI888qgyufV7U6kgFcYV2TDGxsY0V_Lxt5LAHJL8SEn65P-P9YLcBA9PjvuDo6fkFiSqouwBjXbI5ny6sM8gGZynz2sv88nX63bs38Z4chY
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=A+transmission-virulence+evolutionary+trade-off+explains+attenuation+of+HIV-1+in+Uganda&rft.jtitle=eLife&rft.au=Blanquart%2C+Fran%C3%A7ois&rft.au=Grabowski%2C+Mary+Kate&rft.au=Herbeck%2C+Joshua&rft.au=Nalugoda%2C+Fred&rft.date=2016-11-05&rft.eissn=2050-084X&rft.volume=5&rft_id=info:doi/10.7554%2FeLife.20492&rft_id=info%3Apmid%2F27815945&rft.externalDocID=27815945
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2050-084X&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2050-084X&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2050-084X&client=summon