title: Potential drivers of virulence evolution in aquaculture.
abstract: Infectious diseases are economically detrimental to aquaculture, and with continued expansion and intensification of aquaculture, the importance of managing infectious diseases will likely increase in the future. Here, we use evolution of virulence theory, along with examples, to identify aquaculture practices that might lead to the evolution of increased pathogen virulence. We identify eight practices common in aquaculture that theory predicts may favor evolution toward higher pathogen virulence. Four are related to intensive aquaculture operations, and four others are related specifically to infectious disease control. Our intention is to make aquaculture managers aware of these risks, such that with increased vigilance, they might be able to detect and prevent the emergence and spread of increasingly troublesome pathogen strains in the future.
authors.affiliation: Center for Infectious Disease Dynamics Departments of Biology and Entomology The Pennsylvania State University University Park PA USA; Fogarty International Center National Institutes of Health Bethesda MD USA.
authors.forename: David A
authors.initials: DA
authors.lastname: Kennedy
authors.affiliation: U.S. Geological Survey Western Fisheries Research Center Seattle WA USA.
authors.forename: Gael
authors.initials: G
authors.lastname: Kurath
authors.affiliation: Massachusetts Institute of Technology Cambridge MA USA.
authors.forename: Ilana L
authors.initials: IL
authors.lastname: Brito
authors.affiliation: U.S. Geological Survey Western Fisheries Research Center Seattle WA USA.
authors.forename: Maureen K
authors.initials: MK
authors.lastname: Purcell
authors.affiliation: Center for Infectious Disease Dynamics Departments of Biology and Entomology The Pennsylvania State University University Park PA USA; Fogarty International Center National Institutes of Health Bethesda MD USA.
authors.forename: Andrew F
authors.initials: AF
authors.lastname: Read
authors.affiliation: U.S. Geological Survey Western Fisheries Research Center Seattle WA USA.
authors.forename: James R
authors.initials: JR
authors.lastname: Winton
authors.affiliation: Virginia Institute of Marine Science College of William and Mary Gloucester Point VA USA.
authors.forename: Andrew R
authors.initials: AR
authors.lastname: Wargo
keywords: aquaculture; evolution of virulence; infectious diseases
references.citation: Proc Biol Sci. 1999 Feb 22;266(1417):397-404
references.pmid: 10097397
references.citation: J Hered. 2000 Jan-Feb;91(1):35-9
references.pmid: 10739122
references.citation: Proc Biol Sci. 2000 May 22;267(1447):985-90
references.pmid: 10874747
references.citation: J Gen Virol. 2000 Dec;81(Pt 12):2823-32
references.pmid: 11086112
references.citation: Science. 2001 May 11;292(5519):1109-12
references.pmid: 11352066
references.citation: Nature. 2001 Dec 13;414(6865):751-6
references.pmid: 11742400
references.citation: Fish Shellfish Immunol. 2002 Apr;12(4):287-301
references.pmid: 12049167
references.citation: Proc Biol Sci. 2002 Jul 7;269(1498):1317-23
references.pmid: 12079653
references.citation: Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12959-62
references.pmid: 12244216
references.citation: Trends Microbiol. 2003 Jan;11(1):15-20
references.pmid: 12526850
references.citation: Science. 2003 Mar 14;299(5613):1735-7
references.pmid: 12637745
references.citation: J Gen Virol. 2003 Apr;84(Pt 4):803-14
references.pmid: 12655081
references.citation: Dis Aquat Organ. 2003 Aug 4;55(3):175-85
references.pmid: 13677504
references.citation: J Gen Virol. 2004 May;85(Pt 5):1167-79
references.pmid: 15105533
references.citation: Fish Shellfish Immunol. 2004 May;16(5):571-9
references.pmid: 15110331
references.citation: Evolution. 2004 Mar;58(3):455-69
references.pmid: 15119430
references.citation: Am Nat. 2004 Apr;163(4):E40-63
references.pmid: 15122509
references.citation: PLoS Biol. 2004 Sep;2(9):E230
references.pmid: 15221031
references.citation: Parasitol Today. 1996 Mar;12(3):96-101
references.pmid: 15275238
references.citation: Prev Vet Med. 2005 Feb;67(2-3):223-35
references.pmid: 15737433
references.citation: Expert Rev Vaccines. 2005 Feb;4(1):89-101
references.pmid: 15757476
references.citation: Proc Natl Acad Sci U S A. 2005 May 24;102(21):7624-8
references.pmid: 15894623
references.citation: Fish Shellfish Immunol. 2006 Feb;20(2):126-36
references.pmid: 15939627
references.citation: Annu Rev Phytopathol. 2005;43:83-116
references.pmid: 16078878
references.citation: Vet Microbiol. 2006 Oct 5;117(1):14-8
references.pmid: 16698199
references.citation: J Fish Dis. 2006 Jun;29(6):339-46
references.pmid: 16768714
references.citation: Lett Appl Microbiol. 2006 Aug;43(2):137-42
references.pmid: 16869895
references.citation: Ecol Lett. 2006 Aug;9(8):933-40
references.pmid: 16913936
references.citation: Evolution. 2006 Jul;60(7):1358-71
references.pmid: 16929653
references.citation: Arch Virol. 2007 Jan;152(1):151-79
references.pmid: 16941061
references.citation: Fish Shellfish Immunol. 2007 May;22(5):510-9
references.pmid: 17085058
references.citation: J Anim Sci. 2007 Feb;85(2):305-13
references.pmid: 17235017
references.citation: Vet Microbiol. 1991 Nov;29(3-4):289-97
references.pmid: 1771752
references.citation: Evolution. 2007 Sep;61(9):2154-64
references.pmid: 17767587
references.citation: J Anim Sci. 1991 Oct;69(10):4201-8
references.pmid: 1778836
references.citation: J Antimicrob Chemother. 2008 Jun;61(6):1229-33
references.pmid: 18367460
references.citation: Proc Natl Acad Sci U S A. 2008 May 27;105(21):7489-94
references.pmid: 18492806
references.citation: Fish Shellfish Immunol. 2008 Sep;25(3):213-21
references.pmid: 18603444
references.citation: Vaccine. 2008 Sep 8;26(38):4885-92
references.pmid: 18672016
references.citation: Vaccine. 2008 Jul 18;26 Suppl 3:C4-7
references.pmid: 18773527
references.citation: Vaccine. 2008 Jul 18;26 Suppl 3:C42-52
references.pmid: 18773536
references.citation: Malar J. 2008 Dec 16;7:257
references.pmid: 19087299
references.citation: Mar Biotechnol (NY). 2009 Sep-Oct;11(5):570-84
references.pmid: 19139958
references.citation: Avian Pathol. 2000 Jun;29(3):175-94
references.pmid: 19184804
references.citation: J Evol Biol. 2009 Feb;22(2):245-59
references.pmid: 19196383
references.citation: BMC Evol Biol. 2009 Mar 25;9:65
references.pmid: 19320981
references.citation: Philos Trans R Soc Lond B Biol Sci. 2009 Jun 12;364(1523):1555-65
references.pmid: 19414470
references.citation: Am Nat. 2009 Jul;174 Suppl 1:S43-53
references.pmid: 19441961
references.citation: Fish Shellfish Immunol. 2010 Jan;28(1):98-105
references.pmid: 19819334
references.citation: J R Soc Interface. 2010 May 6;7(46):811-22
references.pmid: 19864267
references.citation: Proc Biol Sci. 2010 Feb 22;277(1681):593-600
references.pmid: 19864284
references.citation: J Fish Dis. 2010 Apr;33(4):321-9
references.pmid: 20059633
references.citation: Vet Res. 2010 Nov-Dec;41(6):51
references.pmid: 20409453
references.citation: Virology. 2010 Aug 15;404(1):51-8
references.pmid: 20494388
references.citation: Evol Biol. 2010 Sep;37(2-3):59-67
references.pmid: 21151485
references.citation: Fish Shellfish Immunol. 2011 Jul;31(1):1-9
references.pmid: 21232605
references.citation: Trends Ecol Evol. 1992 Dec;7(12):405-8
references.pmid: 21236081
references.citation: Trends Ecol Evol. 1996 Feb;11(2):79-82
references.pmid: 21237766
references.citation: J Virol. 2011 Apr;85(8):3959-67
references.pmid: 21307204
references.citation: Epidemics. 2011 Mar;3(1):1-11
references.pmid: 21420655
references.citation: Appl Environ Microbiol. 2011 May;77(10):3493-9
references.pmid: 21441334
references.citation: Ecol Lett. 2011 Sep;14(9):841-51
references.pmid: 21699641
references.citation: Science. 2011 Jul 8;333(6039):216-8
references.pmid: 21737739
references.citation: BMC Vet Res. 2011 Nov 11;7:70
references.pmid: 22078942
references.citation: J Invertebr Pathol. 2012 Jun;110(2):247-50
references.pmid: 22434005
references.citation: Curr Opin Virol. 2011 Jul;1(1):73-80
references.pmid: 22440571
references.citation: J Math Biol. 2013 May;66(6):1123-53
references.pmid: 22461126
references.citation: Trends Microbiol. 2012 Jul;20(7):336-42
references.pmid: 22564248
references.citation: PLoS Biol. 2012;10(7):e1001368
references.pmid: 22870063
references.citation: J Aquat Anim Health. 2012 Sep;24(3):141-7
references.pmid: 22870893
references.citation: Proc Biol Sci. 2012 Nov 22;279(1747):4677-85
references.pmid: 23015626
references.citation: Evolution. 2013 Mar;67(3):851-60
references.pmid: 23461333
references.citation: PLoS Biol. 2013;11(5):e1001570
references.pmid: 23723736
references.citation: Front Microbiol. 2013 Aug 22;4:233
references.pmid: 23986749
references.citation: Fish Shellfish Immunol. 2013 Dec;35(6):1683-8
references.pmid: 24099805
references.citation: Dis Aquat Organ. 2013 Dec 12;107(2):99-111
references.pmid: 24334352
references.citation: PLoS Biol. 2015 Jul 27;13(7):e1002198
references.pmid: 26214839
references.citation: Parasitology. 2016 Jun;143(7):915-30
references.pmid: 26302775
references.citation: J Aquat Anim Health. 2006 Dec;18(4):232-43
references.pmid: 26599159
references.citation: Evolution. 1996 Oct;50(5):1729-1741
references.pmid: 28565576
references.citation: Evolution. 1999 Jun;53(3):689-703
references.pmid: 28565637
references.citation: Evolution. 1994 Oct;48(5):1423-1437
references.pmid: 28568406
references.citation: Ann N Y Acad Sci. 1987;503:295-306
references.pmid: 3304078
references.citation: Proc R Soc Lond B Biol Sci. 1983 Jun 22;218(1212):259-85
references.pmid: 6136042
references.citation: Proc R Soc Lond B Biol Sci. 1983 Oct 22;219(1216):281-313
references.pmid: 6139816
references.citation: Parasitology. 1982 Oct;85 (Pt 2):411-26
references.pmid: 6755367
references.citation: J Theor Biol. 1983 Feb 7;100(3):411-26
references.pmid: 6834864
references.citation: Proc Biol Sci. 1994 Jan 22;255(1342):81-9
references.pmid: 8153140
references.citation: Trends Microbiol. 1994 Mar;2(3):73-6
references.pmid: 8156274
references.citation: Vet Res. 1995;26(5-6):361-8
references.pmid: 8581007
references.citation: Q Rev Biol. 1996 Mar;71(1):37-78
references.pmid: 8919665
references.citation: Avian Dis. 1997 Jan-Mar;41(1):149-63
references.pmid: 9087332
references.citation: Science. 1998 Nov 20;282(5393):1432-5
references.pmid: 9822369