AquaBreeding Project title: “Towards enhanced and sustainable use of genetics and breeding in the European aquaculture industry”




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Review on Breeding and Reproduction of European aquaculture species

Brown trout (Salmo trutta)



Marc Vandeputte (INRA, France)


January 2008

1. General information on production and breeding

History of the domestication

Brown trout is perhaps the first species of fish in which artificial reproduction was performed. This was first done by Jacobi in Germany, probably around 1739, and the earliest brown trout hatchery was established in 1841 by Boccius in Hammersmith, UK [1]. The technique of artificial fertilization was optimized by Coste in the 1850s [1]. Since then, brown trout has been produced extensively in Europe and introduced to other continents; but it has never been specifically domesticated for food fish production, as the principal aim of brown trout culture has always been restocking of natural waters. Only briefly, at the end of the 1980s, was the culture of brown trout in sea cages considered as an alternative to salmon production in the French waters of Brittany [2]. This led to the development of brown trout strains selected for fast growth [3].


Production

No FEAP or FAO data is available on brown trout production.


Biological features of interest for breeding practices

  • Main commercial data on weight and age at harvest and slaughtering performances

For restocking, mostly eggs and fingerlings are used. A small amount of production is sold as food fish, usually at portion size (250-350 g), which can be reached in 12 to 18 months post-fertilisation. At large sizes (2 kg or more) yields exceed those of rainbow trout: gutted yield 92% vs. 85%, trimmed and skinned fillet yield 55% vs. 39% (Bugeon et al, unpublished data).

  • Generation interval for males and females

Age at puberty is 1-3 years for males, 2-4 years for females.
Main diseases

Brown trout is affected by several bacterial diseases: it is highly sensitive to furonculosis (Aeromonas salmonicida [4]),and bacterial kidney disease (Renibacterium salmoninarum), but may also suffer moderately from yersiniosis (Yersinia ruckeri [5]), rainbow trout fry syndrome (Flavobacterium psychrophilum [6]), and vibriosis (Vibrio spp. ). A vaccine exists for furonculosis and vibriosis.

The main viral diseases affecting brown trout are VHS (Viral Haemorrhagic Septicaemia), IHN (Infectious Haematopoietic Necrosis) and IPN (Infectious Pancreatic Necrosis). The first two are diseases requiring notification of the authorities, according to the EU Council Directive 91/67/EEC defining Approved Zones free of such diseases. Brown trout are moderately susceptible to pancreas disease, caused by a salmonid alphavirus [7,8]

Brown trout may also suffer from fungal infections (Saproleignia spp), especially during the reproductive season when males are particularly sensitive, and parasitic infections by Costia spp. [4].



2. Genetic variability of the species

Wild genetic resources available (Figure 1)

As brown trout is the native species of trout in Europe, many wild populations of this species exist. Population genetics studies have identified five main lineages: Atlantic, Mediterranean, Adriatic, Danubian and the subspecies Salmo trutta marmoratus [9-12]. Resident and sea migrating ecotypes coexist (except in southern Atlantic and Mediterranean sea [13]), with little or no genetic differentiation between them [14-16].



Figure 1: Native distribution of brown trout (red) and distribution of sea-trout (green). According to Elliott 1994 [13].
Differences between wild and/or domesticated populations

The zootechnical comparison of five domesticated French strains with one domesticated Danish population, one wild French population from Brittany, and some crosses between these groups showed that the domesticated populations had better early survival rates and growth rates than the wild ones [12]. Even among the domesticated fish, considerable variation for growth rate existed both in fresh water (≈50% of the mean) and in sea water (≈30% of the mean).


Interaction between wild and domesticated stocks

Interactions between wild and domesticated stocks have been extensively studied in brown trout, especially in the Mediterranean area, where restocking with Atlantic populations has taking place for a long time [17,18]. It appears in many cases that stocked trout, even if restocked at very young stages, are more vulnerable to angling than wild trout [19,20]. The admixture of domesticated trout in heavily restocked rivers may remain remarkably low, but this is highly variable among situations and in some cases high admixture proportions are observed [21,22]. Even when wild parents are used, reduction in effective population size appears to be common [23].


Inbreeding effects

Not documented.



3. Reproduction

Fecundity and main reproductive features

Brown trout show an egg production of 1000 to 2000 eggs/kg female. Artificial fertilization is easy.


Cryopreservation

Cryopreservation protocols for brown trout sperm exist [24-26]. Thawed sperm give variable but sometimes very high fertilization rates (27-95%).


Genetic and environmental sex determination, sexual dimorphism

XX/XY sex determinism has been demonstrated by meiotic gynogenesis [27]. Neomales may be produced by an early methyltestosterone treatment, but have non functional testes that make the use of intra-testicular sperm the only method possible for producing monosex female populations [27].



4. Selection

Genetic variability per trait

Brown trout was one of the first species in which variation of quantitative traits was studied, a study in 1919 demonstrated heritability of vertebrae number [28]. However, since then, only a few traits have been extensively studied. Skin pigmentation shows good heritability, both for the number of black spots in the dorsal area (h²=0.40 [29]) and for the number of red spots (h²=0.67-0.73 [12,30]). Among other “exotic” traits, number of pyloric caeca [31], and swimming performance [32] have also shown some degree of genetic determinism. The genetics of growth rate has been studied through selective breeding, revealing a realized heritability around 0.3-0.5 [3], which is still quite variable between strains [33]. Genetic variation for growth at the larval stage is mainly determined by maternal effects linked to egg size [34].


Genetic correlations and undesirable side effects

Genetic correlations with growth rate have been studied through the observation of correlated responses to selection for growth on processing yields and quality traits ([35], Vandeputte et al, unpublished data). These studies show little or no effects of selection for growth rate on carcass and fillet yield, flesh fat content or texture. No correlated response is seen on feed efficiency [36,37], but feeding behaviour is clearly altered by selection for growth [38,39].



G*E interactions

Not documented


Genetic responses, progresses and control lines

The “Prosper” program, an optimized mass selection procedure followed for four generations in France, caused a weight increase of 21.5% at 1 year of age in one line, when compared with an unselected control line from the same base population [3]. In a second line however, the response was only 6.3% per generation. This may be a result of differing selection environments: if the one where the response was lower was more competitive, it could have led to the selection of more aggressive fish [33].


Dominance and intraspecific crossing

Crosses between wild and domesticated strains gave performances that were intermediate between the parental strains [12]. Dominance appears to have a significant impact on larval growth (d²=0.34-0.39) [34].



5. Polyploidisation and monosexing and hybrids

Triploid induction and performances

Early trials produced either relatively low proportions of triploids [40] or low survival rates [41]. Using a 28°C heat shock for 10 minutes led both to >90% triploids and hatching rates equivalent to the control [27]. Triploid females exhibit no reduced growth compared with maturing diploid females, and have better carcass yields, 90.6 vs. 81.5% at 4 years in sea water [12], due to their total absence of maturation and gonad development.


Tetraploid induction and performances

Not documented.


Gynogenesis, androgenesis and mitotic clone performances

Only meiotic gynogenesis has been performed in brown trout, using the same shock as for triploid induction [27,42].


Interspecific hybridisation

Diploid hybrids have been made with brook trout (Salvelinus fontinalis) and, though these performed well in fresh water [43], they were not suited to sea water [44], and were therefore never used in practice. Hybrids with rainbow trout are not viable in the diploid state, but can be produced as allotriploids [40,45]. Their performances are not however sufficient for them to be of practical use [46].



6. Genomics

Tools to evaluate population genetic variability

Allozymes, mtDNA and microsatellites have been used to describe the genetic variability of brown trout (e.g. [9;10;23]) A SNP multiplex allowing the distinction of the five main lineages has also recently been produced [47].


Genetic markers for genealogical traceability

The number of microsatellites available (at least 288 polymorphic ones [48]) would clearly allow their usage for parentage assignment. However, no multiplex has been published, and no laboratories perform commercial parentage assignment for this species.


QTL and Marker Assisted Selection

A genetic map has been made with 288 microsatellites and 13 allozymes [48], but no QTL detection program has yet been set up in brown trout.


Transgenesis

No transgenic brown trout have ever been produced.



References

[1] M. Coste, Instructions pratiques sur la pisciculture, suivies de mémoires et de rapports sur le même sujet. Paris: Librairie Victor Masson, 1853, pp. 1-140.

[2] E. Quillet, B. Chevassus, F. Krieg, and G. Burger, "Données actuelles sur l'élevage en mer de la truite commune (Salmo trutta)," La Pisciculture Française, vol. 86, pp. 48-56, 1986.

[3] B. Chevassus, E. Quillet, F. Krieg, M. G. Hollebecq, M. Mambrini, A. Faure, L. Labbe, J. P. Hiseux, and M. Vandeputte, "Enhanced individual selection for selecting fast growing fish: the "PROSPER" method, with application on brown trout (Salmo trutta fario)," Genet. Sel. Evol., vol. 36, pp. 643-661, 2004.

[4] E. Quillet, A. Faure, B. Chevassus, F. Krieg, Y. Harache, J. Arzel, R. Metailler, and G. Boeuf, "The potential of brown trout (Salmo trutta L.) for mariculture," Buvisindi Icel. Agric. Sci., vol. 6, pp. 63-76, 1992.

[5] I. Altinok and J. M. Grizzle, "Effects of Salinity on Yersinia ruckeri Infection of Rainbow Trout and Brown Trout," J. Aquat. Anim. Health, vol. 13, no. 4, pp. 334-339, Dec.2001.

[6] R. C. Cipriano and R. A. Holt, "Flavobacterium psychrophylum, casue of bacterial cold-water disease and rainbow trout fry syndrome,,” 86 ed 2005, pp. 1-44.

[7] P. Boucher, R. S. Raynard, G. Houghton, and F. Baudin Laurencin, "Comparative experimental transmission of pancreas disease in Atlantic salmon, rainbow trout and brown trout," Dis. Aquat. Org., vol. 22, pp. 19-24, 1995.

[8] M. F. McLoughlin and D. A. Graham, "Alphavirus infections in salmonids - a review," J. Fish Dis., vol. 30, no. 9, pp. 511-531, Sept.2007.

[9] L. Bernatchez, "The evolutionary history of brown trout (Salmo trutta L.) inferred from phylogeographic, nested clade, and mismatch analyses of mitochondrial variation," Evolution, vol. 55, no. 2, pp. 351-379, Feb.2001.

[10] F. Krieg and R. Guyomard, "Population genetics of French brown trout (Salmo trutta L.): large geographical differentiation of wild populations and high similarity of domesticated stocks," Genet. Sel. Evol., vol. 17, pp. 225-242, 1985.

[11] R. Guyomard, "Diversité génétique de la truite commune," Bull. Fr. Pêche. Piscic., vol. 314, pp. 146-168, 1989.

[12] B. Chevassus, F. Krieg, R. Guyomard, J. M. Blanc, and E. Quillet, "The genetics of brown trout: twenty years of French research," Buvisindi Icel. Agric. Sci., vol. 6, pp. 109-124, 1992.

[13] J. M. Elliott, Quantitative ecology and the brown trout. Oxford: Oxford University Press, 1994, pp. 1-304.

[14] K. Hindar, B. Jonsson, N. Ryman, and G. Stahl, "Genetic relationships among landlocked, resident, and anadromous brown trout, Salmo trutta L.," Heredity, vol. 66, pp. 83-91, 1991.

[15] T. F. Cross, C. P. R. Mills, and M. Courcy Williams, "An intensive study of allozyme variation in freshwater resident and anadromous trout, Salmo trutta L., in western Ireland*," J. Fish Biol., vol. 40, no. 1, pp. 25-32, Jan.1992.

[16] E. Petersson and T. Jarvi, "Growth and social interactions of wild and sea-ranched brown trout and their hybrids," J. Fish Biol., vol. 63, no. 3, pp. 673-686, 2003.

[17] R. Guyomard and F. Krieg, "Mise en évidence d'un flux génique entre populations naturelles de truite fario et souche de repeuplement dans deux rivières de Corse," Bull. Fr. Pêche. Piscic., vol. 303, pp. 134-140, 1986.

[18] A. Barbat-Leterrier, R. Guyomard, and F. Krieg, "Introgression between introduced domesticated strains and mediterranean native populations of brown trout (Salmo trutta L.)," Aquat. Living Resour., vol. 2, pp. 215-223, 1989.

[19] A. Champigneulle and S. Cachera, "Evaluation of large-scale stocking of early stages of brown trout, (Salmo trutta), to angler catches in the French-Swiss part of the River Doubs," Fish. Manage. Ecol., vol. 10, no. 2, pp. 79-85, Apr.2003.

[20] M. Mezzera and C. R. Largiader, "Evidence for selective angling of introduced trout and their hybrids in a stocked brown trout population," J. Fish Biol., vol. 59, pp. 287-301, 2001.

[21] M. M. Hansen, "Estimating the long-term effects of stocking domesticated trout into wild brown trout (Salmo trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples," Mol. Ecol., vol. 11, no. 6, pp. 1003-1015, 2002.

[22] C. R. Largiader and A. Scholl, "Genetic introgression between native and introduced brown trout Salmo trutta L. populations in the Rhône River Basin," Mol. Ecol., vol. 5, no. 3, pp. 417-426, June1996.

[23] M. M. Hansen, E. E. Nielsen, D. E. Ruzzante, C. Bouza, and K. L. D. Mensberg, "Genetic monitoring of supportive breeding in brown trout (Salmo trutta L.), using microsatellite DNA markers," Can. J. Fish. Aquat. Sci., vol. 57, pp. 2130-2139, 2000.

[24] C. Labbe and G. Maisse, "Characteristics and freezing tolerance of brown trout spermatozoa according to rearing water salinity," Aquaculture, vol. 201, no. 3-4, pp. 287-299, Oct.2001.

[25] K. Sarvi, H. Niksirat, B. Mojazi Amiri, S. M. Mirtorabi, G. R. Rafiee, and M. Bakhtiyari, "Cryopreservation of semen from the endangered Caspian brown trout (Salmo trutta caspius)," Aquaculture, vol. 256, no. 1-4, pp. 564-569, June2006.

[26] F. Lahnsteiner, T. Weismann, and R. A. Patzner, "Methanol as cryoprotectant and the suitability of 1.2 ml and 5 ml straws for cryopreservation of semen from salmonid fishes," Aquacult. Res., vol. 28, no. 6, pp. 471-479, June1997.

[27] E. Quillet, L. Foisil, B. Chevassus, D. Chourrout, and F. G. Liu, "Production of all triploid and all-female brown trout for aquaculture," Aquat. Living Resour., vol. 4, pp. 27-32, 1991.

[28] J. Schmidt, "Racial studies in fishes. III. Diallel crossings with trout (Salmo trutta L.)," J. Genet., vol. 9, pp. 61-67, 1919.

[29] J. M. Blanc, H. Poisson, and R. Vibert, "Variabilité génétique de la ponctuation noire sur la truitelle fario (Salmo trutta L.)," Ann. Genet. Sel. Anim., vol. 14, pp. 225-236, 1982.

[30] J. M. Blanc, "Inheritance of the number of red spots on the skin of the brown trout," Aquat. Living Resour., vol. 7, pp. 133-136, 1994.

[31] J. M. Blanc, B. Chevassus, and P. Bergot, "Déterminisme génétique du nombre de caeca pyloriques chez la truite fario (Salmo trutta, Linné) et la truite arc-en-ciel (Salmo gairdneri, Richardson). III. Effet du génotype et de la taille des oeufs sur la réalisation du caractère chez la truite fario," Ann. Genet. Sel. Anim., vol. 11, pp. 93-103, 1979.

[32] J. M. Blanc and J. F. Toulorge, "Variabilité génétique de la performance de nage chez l'alevin de truite fario (Salmo trutta)," Ann. Genet. Sel. Anim., vol. 13, pp. 165-176, 1981.

[33] B. Chevassus, E. Quillet, F. Krieg, M. G. Hollebecq, M. Mambrini, A. Faure, L. Labbe, J. P. Hiseux, and M. Vandeputte, "Improved mass selection for growth rate in brown trout (Salmo trutta fario): the "PROSPER" process," Aquaculture, vol. 247, p. 8, 2005.

[34] M. Vandeputte, E. Quillet, and B. Chevassus, "Early development and survival in brown trout (Salmo trutta fario L.): indirect effects of selection for growth rate and estimation of genetic parameters," Aquaculture, vol. 204, pp. 435-445, 2002.

[35] S. Bonnet, P. Haffray, B. Chevassus, J. Aubin, and B. Fauconneau, "Conformation and carcass quality traits in seawater adult brown trout: correlated responses to selection for freswater body length, growth and triploidy x selection interactions," Aquaculture, vol. 204, p. 193, 2002.

[36] M. P. Sanchez, B. Chevassus, L. Labbe, E. Quillet, and M. Mambrini, "Selection for growth of brown trout (Salmo trutta) affects feed intake but not feed efficiency," Aquat. Living Resour., vol. 14, no. 1, pp. 41-48, 2001.

[37] M. Mambrini, F. Medale, M. P. Sanchez, B. Recalde, B. Chevassus, L. Labbe, E. Quillet, and T. Boujard, "Selection for growth in brown trout increases feed intake capacity without affecting maintenance and growth requirements," J. Anim. Sci., vol. 82, no. 10, pp. 2865-2875, 2004.

[38] M. Mambrini, M. P. Sanchez, B. Chevassus, L. Labbe, E. Quillet, and T. Boujard, "Selection for growth increases feed intake and affects feeding behavior of brown trout," Livestock Production science, vol. 88, no. 1-2, pp. 85-98, June2004.

[39] T. Boujard, A. Cuvier, I. Geurden, L. Labbe, and M. Mambrini, "Selection for growth and feeding hierarchy in brown trout," Appl. Anim. Behav. Sci., vol. 99, no. 3-4, pp. 344-356, Sept.2006.

[40] P. D. Scheerer and G. H. Thorgaard, "Increased survival in salmonid hybrids by induced triploidy," Can. J. Fish. Aquat. Sci., vol. 40, pp. 2040-2044, 1983.

[41] K. Arai and N. P. Wilkins, "Triploidization of brown trout (Salmo trutta) by heat shocks," Aquaculture, vol. 64, pp. 97-103, 1987.

[42] R. Guyomard, "Gene segregation in gynogenetic brown trout (Salmo trutta L.): systematically high frequencies of post reduction," Genet. Sel. Evol., vol. 18, pp. 385-392, 1986.

[43] J. M. Blanc and B. Chevassus, "Survival, growth and sexual maturation of the tiger trout hybrid (Salmo trutta female x Salvelinus fontinalis male)," Aquaculture, vol. 52, pp. 59-69, 1986.

[44] G. Boeuf and Y. Harache, "Adaptation osmotique à l'eau de mer de différents espèces (Salmo trutta, Salmo gairdneri, Salvelinus fontinalis) et hybrides (Salmo trutta female x salvelinus fontinalis males) de salmonidés," Aquaculture, vol. 40, pp. 343-358, 1984.

[45] B. Chevassus, R. Guyomard, D. Chourrout, and E. Quillet, "Production of viable hybrids in salmonids by triploidisation," Genet. Sel. Evol., vol. 15, pp. 519-532, 1983.

[46] E. Quillet, B. Chevassus, J. M. Blanc, F. Krieg, and D. Chourrout, "Performances of auto and allotriploids in salmonids. 1. survival and growth in freshwater farming," Aquat. Living Resour., vol. 1, pp. 29-43, 1987.

[47] A. P. Apostolidis, P. K. Apostolou, A. Georgiadis, and R. Sandaltzopoulos, " Rapid identification of Salmo trutta lineages by multiplex PCR utilizing primers tailored to discriminate single nucleotide polymorphisms (SNPs) of the mitochondrial control region," Conservation Genetics, vol. 8, pp. 1025-1028, 2007.

[48] K. Gharbi, A. Gautier, R. G. Danzmann, S. Gharbi, T. Sakamoto, B. Hoyheim, J. B. Taggart, M. Cairney, R. Powell, F. Krieg, N. Okamoto, M. M. Ferguson, L. E. Holm, and R. Guyomard, "A Linkage Map for Brown Trout (Salmo trutta): Chromosome Homeologies and Comparative Genome Organization With Other Salmonid Fish," Genetics, vol. 172, no. 4, pp. 2405-2419, Apr.2006.



Review on Breeding and Reproduction of European aquaculture species

Common carp (Cyprinus Carpio L.)


Marc Vandeputte (INRA, France), Otomar Linhart (University of South Bohemia, Czech Republic), Hans Komen (Wageningen University, The Netherlands), Gideon Hulata (Agricultural Research Organization, Israel)


January 20008

1. General information on production and breeding

History of the domestication

Domestication of common carp started 2000 BC in China. Buddhist monks were probably responsible for the distribution of carp from China and Vietnam throughout south–east Asia. In Europe, domestication of carp was started by monasteries in the 12th century AD. The first books on carp culture appeared in the 16th century. Domestication took different directions in China and Europe. In China, ponds were harvested once a year, and the smaller carp were left to reproduce. In Europe, the largest carp were harvested and used for broodstock. Today Chinese and European carp strains differ markedly in growth rate , resistance to crowding and poor water quality, and fertility and fecundity [1, 2]. East-Asian domesticated strains appear to be close to East Asian “wild” strains [3].


Production (Figure 1)

The world production of common carp in 2005 was 3 million tonnes, among which 2.4 originated from China [4]. In Europe (including USSR), the production reached a maximum of 402.000 tonnes in 1990, and decreased steadily in the post-communist times, down to a minimum of 125.000 tonnes in 1997. From then, production increased again moderately, to reach 153.000 tonnes in 2005.



Figure 1. Production countries in the Euro-Mediterranean region.
Biological features of interest for breeding practices

  • Main commercial data on weight and age at harvest and slaughtering performances

Harvest weight is usually between 1 and 2.5 kg, and is reached in 2 to 4 years in European temperate climatic conditions. In tropical countries, production cycles are often much shorter, with fish harvested at much smaller sizes (150-250g) after just a few months of on-growing. In Europe, there is classically a separation between the production of yearlings (10-100g mean weight depending on conditions), which are then stocked into on-growing ponds, for a one to three years on-growing cycle.


  • Generation interval for males and females

In temperate climates, males usually mature at 2 or 3 years, and females at 3 or 4 years. In tropical conditions, this can be 6 months (males) to one year (females), depending on temperature (25ºC to 30 ºC). In the laboratory, with controlled constant temperatures (25ºC) and light regimes (12L/12D), carp males mature after 6 months, and females after 15-24 months [5].
Main diseases

The most problematic diseases are SVC (Spring Viraemia of Carp), which classically produces mortalities in spring, when the fish are weakened by over-wintering, and Koi Herpes Virus (KHV) which is now spreading quickly all around the world, and can cause massive mortalities.


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