Parental genetic diversity of brown trout (Salmo trutta m. fario) brood stock affects offspring susceptibility to whirling disease

Particle and Fibre Toxicology

Dennis Marc Kallert²  György Hoitsy⁴  Gergely Zsigmond³  Csaba Ferenc Guti⁵  Zoltán Tolnai¹  Barbara Forró⁵  Edit Eszterbauer⁵ 

[1]Present address: Semmelweis University, Faculty of Medicine, 26 Üllői út, Budapest, H-1085, Hungary

[2]Present address: Kallert & Loy GbR, 11 Birkenweg, Adelsdorf, 91325, Germany

[3]Szent István University, Faculty of Veterinary Medicine, 2 István utca, Budapest, H-1078, Hungary

[4]Lillafüred Trout Farm, 55 Erzsébet sétány, Miskolc-Lillafüred, H-3517, Hungary

[5]Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungarian Academy of Sciences, 21 Hungária krt, Budapest, H-1143, Hungary

关键词: Myxozoa;    Myxobolus cerebralis;    Microsatellite;    Brood fish;    Phylogeographic lineage;    Relatedness;    Individual inbreeding;   

Others  :  1146798
DOI  :  10.1186/s13071-015-0744-2

 received in 2015-01-21, accepted in 2015-02-16,  发布年份 2015

【 摘 要 】

Background

Whirling disease, caused by the myxozoan parasite Myxobolus cerebralis, has high economical and ecological importance worldwide. Susceptibility to the disease varies considerably among salmonid species. In brown trout (Salmo trutta) the infection is usually subclinical with low mortality, which increases the risk of parasite dissemination, especially when farm fish are used for stocking natural habitats. The influence of intraspecific genetic differences (especially the level of homozygosity) on susceptibility is unknown. Therefore, we examined the possible correlations between parental genetic diversity and offspring susceptibility of brown trout stocks to whirling disease.

Methods

Two brown trout brood stocks from a German and a Hungarian fish farm were genetically characterized using microsatellite and lineage-specific genetic markers. The individual inbreeding coefficient f and pairwise relatedness factor r were estimated based on eight microsatellite markers. Brood stock populations were divided into groups according to low and high f and r value estimates and subjected to selective fertilization. The offspring from these separate groups were exposed to M. cerebralis actinospores, and the infection prevalence and intensity was measured and statistically analysed.

Results

The analysis of phylogeographic lineage heritage revealed high heterogeneity in the Hungarian brood stock since > 50% of individuals were Atlantic-Danubian hybrids, while only pure Atlantic-descending specimens were detected in the German population. Based on f_msat and r_msat estimations, classified non-inbred (NIB), inbred (IB) and a group of closely related fish (REL) were created. The susceptibility of their offspring varied considerably. Although there was no significant difference in the prevalence of M. cerebralis infection, the mean intensity of infection differed significantly between NIB and IB groups. In REL and IB groups, a high variability was observed in infection intensity. No external clinical signs were observed in the exposed brown trout groups.

Conclusions

Our findings indicate that the allelic diversity of brown trout brood stock may constitute a significant factor in disease susceptibility, i.e. the intensity of parasite infection in the subsequent generation.

【 授权许可】

   
2015 Eszterbauer et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Charlesworth D, Charlesworth B. Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Syst. 1987; 18:237-68.
• [2]Falconer DS, Mackay TFC. Introduction to Quantitative Genetics. Longman Group Ltd, Essex; 1996.
• [3]Lynch M, Walsh B. Genetics and Analysis of Quantitative Traits. Sinauer Associates Inc, Sunderland, MA; 1998.
• [4]Kincaid HL. Inbreeding in fish populations used for aquaculture. Aquaculture. 1983; 33:215-27.
• [5]Flagg TA, Waknitz FW, Maynard DJ, Milner GB, Mahnken CVW. The effect of hatcheries on native coho salmon populations in the lower Columbia River. Am Fish Soc Symp. 1995; 15:366-75.
• [6]Wang SZ, Hard J, Utter F. Salmonid inbreeding: a review. Rev Fish Biol Fish. 2002; 11:301-19.
• [7]Tave D. Genetics for Fish Hatchery Managers. AVI Publishing Company Inc, Westport, Connecticut; 1986.
• [8]Withler RE, Beacham TD. Genetic consequences of the simultaneous or sequential addition of semen from multiple males during hatchery spawning of chinook salmon (Oncorhynchus tshawytscha). Aquaculture. 1994; 12:11-23.
• [9]Simon RC. Management techniques to minimize the loss of genetic variability in hatchery fish populations. Am Fish Soc Symp. 1991; 10:487-94.
• [10]Kincaid HL. An evaluation of inbreeding and effective population size in salmonid broodstocks in federal and state hatcheries. Am Fish Soc Symp. 1995; 15:193-204.
• [11]Geiger HA, Smoker WW, Zhivotovsky LA, Gharrett AJ. Variability of family size and marine survival in pink salmon (Oncorhynchus gorbuscha) has implications for conservation biology and human use. Can J Fish Aquat Sc. 1997; 54:2684-90.
• [12]Hard JJ, Connell L, Hershberger WK, Harrell LW. Genetic variation in mortality of chinook salmon (Oncorhynchus tshawytscha) during a bloom of the marine alga Heterosigma akashiwo. J Fish Biol. 2000; 56:1387-97.
• [13]Herman RL. Prevention and control of fish diseases in hatcheries. In: Symposium on diseases of fisheries and shellfishes. Special Publication 5. Snieszko SF, editor. American Fisheries Society, Bethesda, MD; 1970: p.3-15.
• [14]Price DJ. Genetics of susceptibility and resistance to disease in fishes. J Fish Biol. 1985; 26:509-19.
• [15]Chevassus B, Dorson M. Genetics of resistance to disease in fishes. Aquaculture. 1990; 85:83-107.
• [16]Wiegertjes GF, Stet RJM, Parmentier HK, van Muiswinkel WB. Immunogenetics of disease resistance in fish: a comparative approach. Dev Comp Immunol. 1996; 20:365-82.
• [17]Ehlinger NF. Selective breeding of trout for resistance to furunculosis. N Y Fish Game J. 1977; 24:25-36.
• [18]Slierendrecht WJ, Olesen NJ, Juul-Madsen HR, Lorenzen N, Henryon M, Berg P et al.. Rainbow trout offspring with different resistance to viral haemorrhagic septicaemia. Fish Shellfish Immunol. 2001; 11:155-67.
• [19]Ibarra AM, Hedrick RP, Gall GAE. Genetic analysis of rainbow trout susceptibility to the myxosporean Ceratomyxa shasta. Aquaculture. 1994; 120:239-62.
• [20]Nichols KM, Bartholomew J, Thorgaard GH. Mapping multiple genetic loci associated with Ceratomyxa shasta resistance in Oncorhynchus mykiss. Dis Aquat Org. 2003; 56:145-54.
• [21]Schisler GJ, Myklebust KA, Hedrick RP. Inheritance of Myxobolus cerebralis resistance among F1-generation crosses of whirling disease resistant and susceptible rainbow trout strains. J Aquat Anim Health. 2006; 18:109-15.
• [22]Baerwald MR, Petersen JL, Hedrick RP, Schisler GJ, May B. A major effect quantitative trait locus for whirling disease resistance identified in rainbow trout (Oncorhynchus mykiss). Heredity. 2011; 106:920-6.
• [23]Fetherman ER, Winkelman DL, Schisler GJ, Antolin MF. Genetic basis of differences in myxospore count between whirling disease-resistant and susceptible strains of rainbow trout. Dis Aquat Org. 2012; 102:97-106.
• [24]Halliday MM. The biology of Myxosoma cerebralis: the causative organism of whirling disease of salmonids. J Fish Biol. 1976; 9:339-57.
• [25]Hoffman GL. Myxobolus cerebralis, a worldwide cause of salmonid whirling disease. J Aquat Anim Health. 1990; 2:30-7.
• [26]Hedrick RP, El-Matbouli M, Adkison MA, MacConnell E. Whirling disease: re-emergence among wild trout. Immunol Rev. 1998; 166:365-76.
• [27]MacConnell E, Vincent ER. The effects of Myxobolus cerebralis on the salmonid host. In: Whirling disease: Reviews and current topics. American Fisheries Society, Symposium 29. Bartholomew JL, Wilson JC, editors. Bethesda, MD; 2002: p.95-107.
• [28]Fetherman ER, Winkelman DL, Baerwald MR, Schisler GJ. Survival and Reproduction of Myxobolus cerebralis-Resistant Rainbow Trout Introduced to the Colorado River and Increased Resistance of Age-0 Progeny. PLoS One. 2014; 9:e96954.
• [29]Markiw ME. Whirling disease: Earliest susceptible age of rainbow trout to the triactinomyxid of Myxobolus cerebralis. Aquaculture. 1991; 92:1-6.
• [30]Markiw ME. Experimentally induced whirling disease. I. Dose response of fry and adults of rainbow trout exposed to the triactinomyxon stage of Myxobolus cerebralis. J Aquat Anim Health. 1992; 4:40-3.
• [31]El-Matbouli M, Fischer-Scherl T, Hoffmann RW. Present knowledge of the life cycle, taxonomy, pathology, and therapy of some Myxosporea spp. important for freshwater fish. Ann Rev Fish Dis. 1992; 3:367-402.
• [32]Ryce EKN, Zale AV, MacConnell E, Nelson M. Effects of fish age versus size on the development of whirling disease in rainbow trout. Dis Aquat Org. 2005; 63:69-76.
• [33]Hoffman GL. Intercontinental and transcontinental dissemination and transfaunation of fish parasites with emphasis on whirling disease (Myxosoma cerebralis). In: Symposium on diseases of fisheries and shellfishes. Special Publication 5. Snieszko SF, editor. American Fisheries Society, Bethesda, MD; 1970: p.69-81.
• [34]Laikre L, Antunes A, Apostolidis A, Berrebi P, Duguid A, Ferguson A et al.. Conservation genetic management of brown trout (Salmo trutta) in Europe. Report by the concerted action on identification, management and exploitation of genetic resources in the brown trout (Salmo trutta). TROUTCONCERT (EU FAIR CT97–3882). Danmarks fiskeriundersrgelser, Silkeborg; 1999.
• [35]Paladini G, Hansen H, Williams CF, Taylor NGH, Rubio-Mejía OL, Denholm SJ et al.. Reservoir hosts for Gyrodactylus salaris may play a more significant role in epidemics than previously thought. Parasites Vectors. 2014; 7:576. BioMed Central Full Text
• [36]Estoup A, Largiader CR, Perrot E, Chourrout D. Rapid one-tube DNA extraction for reliable PCR detection of fish polymorphic markers and transgenes. Mol Marine Biol Biotech. 1996; 5:295-8.
• [37]Snoj A, Jug T, Melkic E, Susnik S, Pohar J, Dovc P et al.. Mitochondrial and microsatellite DNA analysis of marble trout in Slovenia. J Freshwater Biol (Quaderni ETP). 2000; 29:5-11.
• [38]Bernatchez L. The evolutionary history of brown trout Salmo trutta L. inferred from phylogeographic, nested clade, and mismatch analyses of mitochondrial DNA variation. Evolution. 2001; 55:351-79.
• [39]McMeel OM, Hoey EM, Ferguson A. Partial nucleotide sequences, and routine typing by polymerase chain reaction-restriction fragment length polymorphism, of the brown trout (Salmo trutta) lactate dehydrogenase, LDH-C1-C1*90 and *100 alleles. Mol Ecol. 2001; 10:29-34.
• [40]Marić S, Simonović P, Razpet A. Genetic characterization of brood stock brown trout from Bled fish-farm, Slovenia. Period Biologorum. 2010; 112:145-8.
• [41]Estoup A, Presa P, Krieg F, Vaiman D, Guyomard R. CT)n and (GT)n microsatellites: a new class of genetic markers for Salmo trutta L. (brown trout. Heredity. 1993; 71:488-96.
• [42]Presa P, Guyomard R. Conservation of microsatellites in three species of salmonids. J Fish Biol. 1996; 49:1326-9.
• [43]Slettan A, Olsaker I, Lie Ø. Atlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci. Anim Gen. 1995; 26:281-2.
• [44]O’Reilly PT, Hamilton LC, McConnell SK, Wright JM. Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can J Fisheries Aquat Sci. 1996; 53:2292-8.
• [45]Smith CT, Koop BF, Nelson RJ. Isolation and characterization of coho salmon (Oncorhynchus kisutch) microsatellites and their use in other salmonids. Mol Ecol. 1998; 7:1614-6.
• [46]Wang J. COANCESTRY: A program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resources. 2011; 11:141-5.
• [47]Kallert DM, El-Matbouli M. Differences in viability and reactivity of actinospores of three myxozoan species upon ageing. Folia Parasitol. 2008; 55:105-10.
• [48]Eszterbauer E, Kallert DM, Grabner D, El-Matbouli M. Differentially expressed parasite genes involved in host recognition and invasion of the triactinomyxon stage of Myxobolus cerebralis (Myxozoa). Parasitology. 2009; 136:367-77.
• [49]Rózsa L, Reiczigel J, Majoros G. Quantifying parasites in samples of hosts. J Parasitol. 2000; 86:228-32.
• [50]Keller LF, Waller DM. Inbreeding effects in wild populations. Trends Ecol Evol. 2002; 17:230-41.
• [51]McKay LR, McMillan I, Sadler SE, Moccia RD. Effects of mating system on inbreeding levels and selection response in Salmonid aquaculture. Aquaculture. 1992; 100:100-1.
• [52]Aulstad D, Gjedrem T, Skjervold H. Genetic and environmental sources of variation in length and weight of rainbow trout (Salmo gairdneri). J Fish Res Board Canada. 1972; 29:237-41.
• [53]Gjerde B, Gunnes K, Gjedrem T. Effect of inbreeding on survival and growth in rainbow trout. Aquaculture. 1983; 34:327-32.
• [54]Su GS, Liljedahl LE, Gall GAE. Effects of inbreeding on growth and reproductive traits in rainbow trout (Oncorhynchus mykiss). Aquaculture. 1996; 142:139-48.
• [55]Balloux F, Amos W, Coulson T. Does heterozygosity estimate inbreeding in real populations? Mol Ecol. 2004; 13:3021-31.
• [56]Steinbach Elwell LC, Stromberg KE, Ryce EKN, Bartholomew JL. Whirling Disease in the United States. A summary of progress in research and management 2009. Trout Unlimited and The Whirling Disease Foundation, Bozeman, Montana; 2009.
• [57]El-Matbouli M, Hoffmann RW, Mandok C. Light and electron microscopic observations on the route of the triactinomyxon-sporoplasm of Myxobolus cerebralis from epidermis into rainbow trout cartilage. J Fish Biol. 1995; 46:919-35.
• [58]Hedrick RP, McDowell TS, Gay M, Marty GD, Georgiadis MP, MacConnell E. Comparative susceptibility of rainbow trout Onchorhynchus mykiss and brown trout Salmo trutta to Myxobolus cerebralis, the cause of salmonid whirling disease. Dis Aquat Org. 1999; 37:173-83.
• [59]Baldwin TJ, Vincent ER, Silflow RM, Stanek D. Myxobolus cerebralis infection in rainbow trout (Oncorhynchus mykiss) and brown trout (Salmo trutta) exposed under natural stream conditions. J Vet Diag Invest. 2000; 12:312-21.
• [60]Gómez D, Bartholomew J, Sunyer JO. Biology and mucosal immunity to myxozoans. Dev Comp Immunol. 2014; 43:243-56.