Abstract
We report genetic differences for resistance to the pathogen Listonella anguillarum within and among one cultured and two wild Canadian populations of Atlantic salmon, Salmo salar, using a common-garden experimental protocol. Following exposure to the causative agent for vibriosis, parr originating from the endangered Stewiacke River population experienced significantly higher mortality than cultured parr, four generations removed from the Saint John River population, and wild parr from Tusket River. Pathogen resistance differed between sexes; males consistently experienced higher survival than females. There was no evidence that maturity influenced pathogen resistance in male parr. The population and sex differences in pathogen resistance documented here have implications for risk assessments of the demographic consequences of interbreeding between wild and farmed Atlantic salmon.
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Ackerman PA, Iwama GK (2001) Physiological and cellular stress responses of juvenile rainbow trout to vibriosis. J Aquat Anim Health 13:173–180 doi:10.1577/1548-8667(2001)013<0173:PACSRO>2.0.CO;2
Alsina M, Blanch AR (1994) A set of keys for biochemical identification of environmental Vibrio species. J Appl Bacteriol 76:79–85
Amiro PG, Longard DA, Jefferson EM (2000) Assessments of Atlantic salmon stocks of salmon fishing areas 20 and 21, the southern upland of Nova Scotia, for 1999. Canadian Stock Assessment Secretariat Research Document 2000/009. Department of Fisheries and Oceans, Ottawa
Arkush KD, Giese AR, Mendonca HL, McBride AM, Marty GD, Hedrick PW (2002) Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes. Can J Fish Aquat Sci 59:966–975 doi:10.1139/f02-066
Arndt SKA (2000) Influence of sexual maturity on feeding, growth and energy stores of wild Atlantic salmon parr. J Fish Biol 57:589–596 doi:10.1111/j.1095-8649.2000.tb00262.x
Bakke TA, Jansen PA, Hansen LP (1990) Differences in the resistance of Atlantic salmon, Salmo salar L., stocks to the monogenean Gyrodatylus salaris Malmberg, 1957. J Fish Biol 37:577–587
Balfry SK, Heath DD, Iwama GK (1997) Genetic analysis of lysozyme activity and resistance to vibriosis in farmed chinook salmon, Oncorhynchus tshawytscha (Walbaum). Aquaculture 28:893–899 doi:10.1111/j.1365-2109.1997.tb01013.x
Balfry SK, Maule AG, Iwama GK (2001) Coho salmon Oncorhynchus kisutch strain differences in disease resistance and non-specific immunity, following immersion challenges with Vibrio anguillarum. Dis Aquat Organ 47:39–48 doi:10.3354/dao047039
Beacham TD, Evelyn TP (1992) Population and genetic variation in resistance of chinook salmon to vibriosis, furunculosis, and bacterial kidney disease. Anim Health 4:153–167 doi:10.1577/1548-8667(1992)004<0153:PAGVIR>2.3.CO;2
Chevassus B, Dorson M (1990) Genetics of resistance to disease in fishes. Aquaculture 85:83–107 doi:10.1016/0044-8486(90)90009-C
COSEWIC (2006) COSEWIC and status report on the Atlantic salmon Salmo salar (inner Bay of Fundy populations) in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa www.sararegistry.gc.ca/status/status_e.cfm
Crawley MJ (2002) Statistical computing: an introduction to data analysis using S-Plus. Wiley, New York, p 761
Fjålestad KT, Larsen HJS, Røed KH (1996) Antibody response in Atlantic salmon (Salmo salar) against Vibrio anguillarum and Vibrio salmonicida O-antigens: heritabilities, genetic correlations and correlations with survival. Aquaculture 145:77–89 doi:10.1016/S0044-8486(96)01331-2
Fleming IA (1996) Reproductive strategies of Atlantic salmon: ecology and evolution. Rev Fish Biol Fish 6:379–416 doi:10.1007/BF00164323
Ford MJ (2004) Conservation units and preserving diversity. In: Hendry AP, Stearns SC (eds) Evolution illuminated: salmon and their relatives. Oxford University Press, New York, pp 338–357
Fraser DJ, Cook AM, Eddington JD, Bentzen P, Hutchings JA (2008) Mixed evidence for reduced local adaptation in wild salmon resulting from interbreeding with escaped farmed salmon: complexities in hybrid fitness. Evol Applic 1:501–512 doi:10.1111/j.1752-4571.2008-00037.x
Fraser DJ, Lippe C, Bernatchez L (2004) Consequences of unequal population size, asymmetric gene flow and sex-biased dispersal on population structure in brook charr (Salvelinus fontinalis). Mol Ecol 13:67–80 doi:10.1046/j.1365-294X.2003.02038.x
Garcia de Leaniz C, Fleming IA, Einum S, Verspoor E, Jordan WC, Consuegra S et al (2007) A critical review of Adaptive genetic variation in Atlantic salmon: implications for conservation. Biol Rev Camb Philos Soc 82:173–211 doi:10.1111/j.1469-185X.2006.00004.x
Giese AR, Hedrick PW (2003) Genetic variation and resistance to a bacterial infection in the endangered Gila topminnow. Anim Conserv 6:369–377 doi:10.1017/S1367943003003445
Gjedrem T, Aulstad D (1974) Differences in resistance to Vibrio disease of salmon parr (Salmo salar). Aquaculture 3:51–59 doi:10.1016/0044-8486(74)90098-2
Glebe BD (1998) East coast salmon aquaculture breeding programs: history and future. Canadian Stock Assessment Secretariat Research Document 98/157. Department of Fisheries and Oceans, Ottawa
Hemmingsen AR, Holt RA, Ewing RD, McIntyre JD (1986) Susceptibility of progeny from crosses among three stocks of coho salmon to infection by Ceratomyxa shasta. Trans Am Fish Soc 115:492–495 doi:10.1577/1548-8659(1986)115<492:SOPFCA>2.0.CO;2
Hendry AP, Catsric V, Kinnison MT, Quinn TP (2004) The evolution of philopatry and dispersal: homing versus straying in salmonids. In: Hendry AP, Stearns SC (eds) Evolution illuminated: salmon and their relatives. Oxford University Press, New York, pp 52–91
Hutchings JA, Pickle A, McGregor-Shaw CR, Poirier L (1999) Influence of sex, body size, and reproduction on overwinter lipid depletion in brook trout. J Fish Biol 55:1020–1028 doi:10.1111/j.1095-8649.1999.tb00737.x
Hutchings JA, Gerber L (2002) Sex-biased dispersal in a salmonid fish. Proc R Soc Lond B Biol Sci 269:2487–2493 doi:10.1098/rspb.2002.2176
Hutchings JA, Fraser DJ (2008) The nature of fisheries- and farming-induced evolution. Mol Ecol 17:294–313 doi:10.1111/j.1365-294X.2007.03485.x
Johnsen BO, Jensen AJ (1991) The Gyrodactylus story in Norway. Aquaculture 98:289–302 doi:10.1016/0044-8486(91)90393-L
Jonsson N, Jonsson B (2003) Energy allocation among developmental stages, age groups, and types of Atlantic salmon (Salmo salar) spawners. Can J Fish Aquat Sci 60:506–516 doi:10.1139/f03-042
King TL, Kalinowski ST, Schill WB, Spidle AP, Lubinski BA (2001) Population structure of Atlantic salmon (Salmo salar L.): a range-wide perspective from microsatellite DNA variation. Mol Ecol 10:807–821 doi:10.1046/j.1365-294X.2001.01231.x
Lafferty KD, Gerber L (2002) Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conserv Biol 16:593–604 doi:10.1046/j.1523-1739.2002.00446.x
Lang T, Mellergaard S, Wosniok W, Kadakas V, Neumann K (1999) Spatial distribution of grossly visible diseases and parasites in flounder (Platichthys flesus) from the Baltic Sea: a synoptic survey. ICES J Mar Sci 56:138–147 doi:10.1006/jmsc.1999.0465
Lawhavinit O-A, Chukanhom K, Hatai K (2002) Effect of Tetrahymena on the occurrence of achlyosis in the guppy. Mycoscience 43:27–31 doi:10.1007/s102670200005
MacKinnon A-M, Campbell M, Olivier G (1998) Overview of fish disease agents in cultivated and wild salmonid populations in the Maritimes. Canadian Stock Assessment Secretariat Research Document 98/160. Department of Fisheries and Oceans, Ottawa
McConnell SKJ, Ruzzante DE, O’Reilly PT, Hamilton L, Wright JM (1997) Microsatellite loci reveal highly significant genetic differentiation among Atlantic salmon (Salmo salar L.) stocks from the east coast of Canada. Mol Ecol 6:1075–1089 doi:10.1046/j.1365-294X.1997.00282.x
Olivier G, MacKinnon A-M (1998) A review of potential impacts on wild salmon stocks from diseases attributed to farmed salmon operations. Canadian Stock Assessment Secretariat Research Document 98/159. Department of Fisheries and Oceans, Ottawa
O’Reilly PT, Hamilton LC, McConnell SK, Wright JM (1996) Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can J Fish Aquat Sci 53:2292–2298 doi:10.1139/cjfas-53-10-2292
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Roff DA (2002) Life history evolution. Sinauer, Sunderland, MA, p 527
Salmon Genetics Research Program (SGRP) (1985) Annual report, 1984–1985. Huntsman Marine Science Centre, St. Andrews, NB, Canada
Taylor EB (1991) A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98:185–207 doi:10.1016/0044-8486(91)90383-I
Verspoor E, O’Sullivan M, Arnold AL, Knox D, Amiro PG (2002) Restricted matrilineal gene flow and regional differentiation among Atlantic salmon (Salmo salar L.) populations within the Bay of Fundy, eastern Canada. Heredity 89:465–472 doi:10.1038/sj.hdy.6800166
Vethaak AD, Bucke D, Lang T, Wester PW, Jol J, Carr M (1992) Fish disease monitoring along a pollution transect: a case study using dab Limanda limanda in the German Bight. Mar Ecol Prog Ser 91:173–192 doi:10.3354/meps091173
Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159
Acknowledgements
We are extremely grateful to P. Avendaño, J. Eddington, and particularly S. Thompson for assistance in the laboratory. We thank P. Ackerman, University of British Columbia, for providing the strain of L. anguillarum used in our study. For assistance in the collection of broodstock and gametes, we are grateful to B. Glebe (Department of Fisheries and Oceans [DFO], St. Andrews, New Brunswick) for the cultured salmon, and to staff at DFO’s Coldbrook Biodiversity Facility and at DFO’s Bedford Institute of Oceanography, especially D. Aiken, B. Lenetine, S. O’Neil, and P. O’Reilly. L. White (Natural Resources Canada) kindly provided the map from The Atlas of Canada. The research was supported by a grant to JAH from AquaNet, one of Canada’s former National Centres of Excellence, and by a Natural Sciences and Engineering Research Council Discovery Grant to JAH. Funding for AD was provided by the National Research Council of Canada’s Genome and Health Initiative.
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Lawlor, J.L., Dacanay, A., Hutchings, J.A. et al. Differences in pathogen resistance within and among cultured, conservation-dependent, and endangered populations of Atlantic salmon, Salmo salar L.. Environ Biol Fish 84, 69–78 (2009). https://doi.org/10.1007/s10641-008-9390-2
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DOI: https://doi.org/10.1007/s10641-008-9390-2