Breeding for disease resistance of Penaeid shrimps

James Cock a, Thomas Gitterle a, Marcela Salazar a, Morten Rye b,

Aq ua c ul t ur e 2 8 6 (2 00 9 ) 1 –11


 1. Introduction

 the nativespeciesP. mon odon and the introduced species of P. vannamei. Furthermore, P. stylirostris, which represented close to 20% of the neo- Diseases and pestsare major constraintson the supply of high quality tropicalcultivated shrimp production, is now rarely cultivated dueto its plant and animal products underintensive production systems. Growers susceptibility to various viruses (Lightner, 2005b). and researchers have developed a whole series of crop and animal Most of the concepts behind disease control in animal species have husbandry systems geared to minimizing the harmful effects of been developed for warmblooded terrestrial species. However, there are pathogens and pests. Recently Keen et al. (2001) observed the major differences in their environment and that of marine anima ls, commonality in microbial virulence mechanisms and the occurrence indicating that transfer of technology from one to the other should be of similar innate resistance systems in animals and plants with an carried out with caution. Warmblooded terrestrial landanimalsmaintain ancient and intertwined history. Similarly, Toyodaet al. (2002) comment a relatively constant body temperature, whereas shrimps like many other on the remarkable similarityof innate responses to pathogens in plants, aquatic organisms are ectothermal andtheir bodytemperature uctuates insects and mammals. In the particular case of shrimps, cultivation is with that of the water in which they live. Similarly, the composition of the relatively new and there is limited knowledge on response to pathogens. medium in which land animals live, the air, varies little with such vital Hence, where there are major gaps in knowledge specifictoshrimpsor aspects as oxygen and carbon dioxide content relatively constant on a crustaceans, we use experience obtained in both plants and animals as global basis. On the other hand, shrimps face tremendous variability in analogous guidelines. In thefirst section of thearticle wediscuss disease the environment in which they live with dramatic changes often and disease control, particularly geneticallycontrolled host resistance, in occurring abruptly. Stress, which is closely related to the manifestation cultivated shrimp and other species in general terms, and then use this of diseases (Biggs, 1985),isofteninducedbychangesinsuchparameters information to provide guidelines on the circumstances when breeding as temperature, oxygen, salinity and ammonium. Farmers on a dayto day for disease resistance is an appropriate control measure and how basis attempt to control diseases by managing the environment and breeding programmes can be structured. reducing the variability in the aquatic environment. Vaccination is a common disease control measure in warm blooded 2. Diseases in intensive shrimp production systems animals, protecting hundreds of millions of animals from disease and death (NOAH, 2002). Vaccines stimulate the body to produce its own Shrimps have only recently been cultivated by man, and it is only defence against infection. The defensive system “remembers” the been in the last twenty to thirty years that the cultivated populations, identity of invading organisms and combats them when a vaccinated animal is confronted with a specific disease organism. This protects the of some species that are easily reproduced in captivity, have been isolated from wild populations. Consequently, most populations of individual animal and, because this animal will not develop the disease cultivated shrimp haveonly had a relatively short period to evolve and and will not become infective, it will also help protect the population adapt to intensive cultivated production systems. from the disease due to ‘herd immunity’ (NOAH, 2002). It is generally Diseases that remain at a low level of incidence in natural accepted that Crustaceans do not possess the capacity to acquire populations may reach epidemic levels in intensive cultivation systems. resistance and hence vaccination is not possible, although this Intensive management systems in livestock production encourage the assumption is questioned by Witteveldt (2006). unpredictable appearance of new diseases and changes in the characteristics of established diseases (Biggs, 1985). Modern intensive 2.1. Disease avoidance shrimp systems provide almost ideal conditions for the propagation of diseases. In the tropics shrimp are often cultivated year round with no On a global scalesimpleavoidanceof diseases and pestshas been one break in the production cycle. Animals are confined in ponds, tanks or of the most effective means of minimizing damage of cultivated or raceways at high densities, water exchange is limited and moribund cultured species. Crop productivity is normally greater outside the animals are not culled from the system. This latter is of particular centre of origin due to less diseases and pest pressure (Jennings and importance as cannibalism is common, disseminating pathogens Cock,1977). In plants the classic exampleof avoidance outsidethecentre effectively. Furthermore some diseases of shrimps are common to of origin isthesuccess of rubber plantations in South East Asiaand Africa various crustaceans (Wang et al., 2004, 2005; Nunan et al., 2004; Lo due to the absence of South American Leaf Blight, which decimates et al., 1996; Lightner, 2005b) and it is difficult to isolate commercia l intensively cultivated populations in the Amazon basin (Davis, 1996). In production from other crustacean species, such as crabs, or copepods, animal populations there are also large differences in disease incidence that may be alternate hosts of shrimp diseases. All these conditions depending on their geographical locations with introduced species favour epidemics and the appearance of apparently new diseases in facing fewer parasites (Torchin et al., 2003). The success of introduced intensive shrimp production systems. On the Pacific coast of Centraland invasive species is often directly attributable to the lack of pathogens in South America, where a native species, Penaeus vannamei,ismost the new environment. In domesticated animal populations simple widely cultivated, Taura Syndrome Virus (TSV) devastated the industry avoidance of diseases and pests has long been oneof the most important in the early nineties (Brock, 1997). Later White Spot Syndrome Virus means of disease control, with eradication of Newcastle disease in (WSSV) appeared in Asia and rapidly devastated the shrimp industry in poultry and rinderpest and foot and mouth disease in cattle being well many parts of the world. Both of these diseases were previously known cases (Biggs, 1985). unreported. Similarly in Asia White Spot and Yellow Head epidemics Disease avoidance or eradication is only possible in certain have reduced production of various Penaeid shrimp species, including circumstances. Exclusion of diseases has been attempted with some 3 J . C oc k et al . / A qu ac u ltu r e 28 6 (20 09 ) 1 – 1 1 success in shrimp cultivation (McIntosh,1999; Moss, 1999), with various system that protects them from foreign organisms. It is generally programmes emphasising the use of Specific Pathogen Free stock in accepted that they do not have the ability to acquire immunity and breedingprogrammes to minimize spread of diseases (Moss, 1999; Moss hence there is no possibility of developing vaccines for shrimps which et al., 2003; Lightner, 2005a; Hennig et al., 2005). However, it is not easy willprovide longterm immunity to a specific disease. However, recently to avoid or eradicate diseases with an open air aquatic grow-out Witteveldt (2006) indicated that vaccination of shrimp against WSSV environment that is normally close to the sea. McCallum et al. (2004) might be possible which would open the way to the design of new have pointed out that, although the same basic principles apply to the strategies to control WSSV and other invertebrate pathogens. Never- epidemiology of both terrestrial and marine species, there are major theless, this result is questioned by many immunologists. In addition qualitative differences and these affect the management practices for there may be possibilities to stimulate the immune system and a series their control. The life cycles differconsiderably and the rate of spread of of non-specific responses against invading organisms. epidemics appears to bemuch greater in marine environments and they Geneticallycontrolled behavioural characteristics may also provide tend to bemoredevastating (McCallum et al., 2004). With the exception resistance to disease: for example genetically controlled hygienic of some diseases, such as Yellow Head Virus (YHV) and Monodon behaviour in bees prevents chalk brood disease (Milne, 1983). With Bacillus Virus (MBV), most of the shrimp viruses have spread rapidly cannibalism playing such an important role in infection in intensive from the sites where they were first recognised (Lightner 1996, 2005b; shrimp culture, it is possible that genetic control of cannibalistic Flegel et al., 2004). The recent epidemic of White Spot Syndrome behaviour may be involved in providing a measure of resistance to indicates how rapidly an epidemic may spread in marine species: First infection (Gitterle et al., 2005). detected in Taiwan in 1992 (Chou et al., 1995), WSSV rapidly spread to With diseases that are difficult to eradicate, control measures have most Asian countries (Inouye et al., 1994; Zhan et al., 1998; Flegel and been developed based on stimulation or enhancement of the natural Alday-Sanz, 1998; Wongteerasupaya et al., 1995) and by 1996 most defencemechanisms of the host organism, including selection for host shrimp farming regions in South East Asia were affected (Flegel and resistance or tolerance to diseases and modification of the environ- Alday-Sanz, 1998). In thewestern hemisphere the first outbreak of WSSV ment so that the disease is not favoured. In plants conscious selective appeared in farmed P. vannamei and P. stylirostris in South Carolina breeding for host resistance or tolerance to diseases dates back to (USA) in 1997 and it was associated with 95% cumulative losses approximately the middle of the twentieth century, whereas (Lightner, 1999). By early 1999, WSSV had spread to farmed P. vann amei conscious selective breeding schemes for livestock disease resistance in Central America (Jory and Dixon, 1999) reachingtheColombian Pacific is more recent and in the case of Penaeid shrimps selective breeding coast in May of that year. The diseases devastated most of the major for resistance was initiated in the 1990s. shrimp producing areas of the world. Attempts to eradicate or exclude the disease were mostly unsuccessful. White Spot Syndrome Virus 3. Disease resistance appeared to have been successfully excluded from a few shrimp producing regions, particularly the Atlantic coast of South America; Genetically based host resistance is an attractive proposition from however it has recently been reported in thecooler temperatureregions the point of view of the grower of improved stock. The grower, apart of southern Brazil (Anon, 2005). It now appears that conditions on the from paying for the resistant genetic stock, does not have to make Atlantic coast of South America were in general not conducive to the further major outlays, although management practices that allow the development of full scaleWhite Spot due to thehigh water temperatures resistance to be expressed may be required. A further advantage of (Vidal et al., 2001). The lack of White Spot Virus epidemics in this area host resistance is the minimal negative impact on the environment as appears to be related to the virus’s inability to replicate at the higher neither antibiotics nor chemical treatments are normally needed to temperature rather than a temperature mediated response by the enhance control. On the other hand development of genetically based shrimp (Reyes et al., 2007). Some areasin South and South East Asiamay host resistance is often costly and may be impossible to achieve in the have escaped or have low incidence of WSSV due to higher water absence of useful levels of resistance. Furthermore, each characteristic temperatures. Shrimp farmers have in some cases reduced water that is added to a selective breeding program inevitably leads to exchange and appear to have achieved some level of control of WSSV slower progress in other desirable characteristics in the breeding goal. with this practice, which probably both increases water temperatures Added to this, disease resistance may be negatively associated with and also reduces the chances of pathogens entering the ponds. other desirable characteristics. These associations may be genetically Furthermore, in Thailand the use of Specific Pathogen Free (SPF) stocks linked to genes that are close to each other on the same chromosome, and bio-security measures have reduced WSSV incidence dramatically or there may be a metabolic, physiological or ecological cost of the (anonymous reviewer, pers. comm.). On the other hand, on the Pacific resistance. Selective breeding for resistance is an attractive option for Coast of the neo-tropics WSSV SPFs and other bio-security measures managing diseases, but it is not a panacea for control of all diseases. In have not markedly reduced disease incidence. Thus, although it is order to justify the high cost of developing genetically disease generally difficult to avoid diseases in cultivated shrimps through resistant populations this approach is only advisable when: (a) the elimination of the causal agent or the use of Specific Pathogen Free disease causes severe damage; (b) there are no other existing simple stocks, it may be possible in certain circumstances to use these cost effective control measures; and (c) there is demonstrable genetic approaches to reduce incidence: in the particular case of WSSV the variation in resistance and this is not coupled with an excessive level avoidance of disease epidemics in the neo-tropics is largely based on of negative associations with other desirable characteristics. finding conditions not suitable for the development of the organism, rather than through elimination of the causal agent itself. 3.1. Evolution of genetic disease resistance 2.2. Host response and resistance to diseases Selection for disease resistance under natural conditions depends on both the advantages that ensue from being able to combat Shrimps have evolved under conditions that are favourable for infections and also the costs of maintaining defences in the absenceof infection and have developed a series of defence mechanisms that infection (Kraaijeveld and Godfray, 1997; Coustau et al., 2000). There protect them from infectious diseases in their native habitat. Disease are a small number of genetic improvement programmes with the resistance in many animals is mediated by both innate and acquired species that were first bred in captivity (P. stylirostris and P. vannamei) resistance. Innate immunity is rapid, non-specific and acts as a first line that have passed through many generations (Goyard et al., 2002; of defence, whileacquired resistance involvesantigen specific responses Wyban et al., 1992). However, the Penaeid shrimp populations used in (Bishop et al., 2002). Shrimps, ascrustaceans, possess an innateimmune most breeding programs are only, at the most, a few generations 4 J . Co ck et a l. / A qu ac u l tur e 2 86 (2 00 9) 1– 1 1 removed from the native populations from which they were natural selection in the field with larger genetic variation and extremely developed and hence levels of disease resistance will tend to re ect high mortalities (well over 99%) are likely to uncover single gene the balance between the advantages and costs under natural resistance which will normally be dominant. conditions, unless selection pressure for disease resistance under Initially in plants horizontal resistance or polygenic resistance was cultivated conditions has been strong. considered to be durable, and vertical (gene for gene or single gene) The genetic control of disease resistance in shrimps is not well resistance was subject to breakdown as thealteration of one genein the understood and little research has been dedicated to the theme until pathogens was sufficient to overcome the one gene conferring very recently. As noted previously, shrimps appear to have no acquired resistance in the vertical gene-for-gene resistance. As Zadoks (2002) immune response, and in this sense they are perhaps somewhere points out, most of the concepts related to vertical and horizontal between plants and mammals in their response, and certainly with resistance have been modified: single gene resistance can be durable some interesting comparisons with invertebrates in general. Unfortu- and polygenic resistance can be eroded or worn down. The most widely nately the information on genetic control of disease resistance in cited examples of durable resistance against bacterial and fungal invertebrates is also limited. Consequently we draw inferences on pathogens in plants are quantitative traits (Leach, 2001). Nevertheless, various aspects of genetic control of disease resistance in other species, there are a few cases where single gene partial resistance has been particularly plants and mammals in which there is a vast stock of durable in plants and it appears that this occurs when the cost to the knowledge. Selective breeding for disease resistance in plants has a pathogen of overcoming the resistance is high (Leach, 2001; Hulbert longer trajectory than in mammals. The early work on host plant et al., 2001). Nevertheless the tendency in plant breeding has moved resistance divided resistance broadly into two categories (see for from breeding for vertical resistance to breeding for horizontal example Van der Planck, 1963, 1968; Zadoks, 2002). In simple terms resistance or pyramiding of single genes as a means of making break- vertical resistant provided effective immunity, normally through down of resistance less likely(seefor example Pink, 2002; Pederson and hypersensitivity, somewhat similar to apoptosis in animals, and was Leath, 1988). controlled by single genes. Horizontal resistance did not provide total Disease resistance in most animals that have been studied is immunity but slowed the spread of the disease and was controlled by controlled quantitatively by many genes and in breeding programmes many genes. it is generally assumed that disease resistance is a quantitative trait Recently, whilst reviewing invertebrateimmunology, Rolff and Siva- under the control of many genes (see for example Detilleux, 2001). Jothy (2003) indicate that when selection pressure is strong, resistance Nevertheless there are recorded cases of single gene resistance in may be monogenic and when selection pressure is lower polygenic. animals and humans (Hill, 2001) and breeders should not ignore the Similarly, Coustau et al. (2000) indicate that when there is a new possibility of using them to confer resistance. At the same time we note environment inwhich the current phenotypesarenot viable, theoretical that most animal breeding programmes and studies of the genetics of considerations suggest that single major mutations are likely to be resistance have been developed with species in which screening of involved in adaptation to the new environment. Although Orrand Coyne millions of animals for disease resistance is simply not possible. The (1992) suggest that responses to pathogens are more likely to be mind simply boggles at inoculation and subsequent screening of several polygenic with small effects, Orr (1998) indicates that long term million cows to see if just one possesses a single gene for resistance to evolution often involves the fixation of mutations of large effect. We mastitis. On theother hand plant breeders regularly inoculate hundreds suggest that in shrimps entering a new environment under intensive of thousands of plants to identify and select resistant materials. cultivated systems and with the extremely high selection pressure in the Furthermore, in the case of the development of pesticide resistance in case of diseases such as WSSV, which kill 98% or more of the population insects and acaroids millions of individuals were subjected to the in severe epidemics (Lightner, 1996; Vidal et al., 2001), monogenic equivalent of screening for the very few resistant genotypes every time resistance or resistance under the control of a small number of genes farmers applied insecticides to their commercial plantations. In the case may arise. Certainly resistance to antibiotics in bacteria (Mazel and of shrimps a single hatchery can easily produceseveral million nauplii in Davies, 1999) and to insecticides in insect populations (Roush and a day and could expose millions of larvae or subsequent stages to a McKenzie, 1987), where selection pressure is extremely high, is disease within few days or at the most weeks and select any survivors. frequently conferred by single genes. This seems obvious when one Hence, wesuggest that usefulsingle generesistancewhich is likelyoccur considers that in the case of catastrophic circumstances, in which all for pathogens that cause severe mortalities, but that they may exist in susceptible organisms die, there is little chance for the slow accumula- very low frequencies, could well be identified in shrimps and may tion of polygenic resistance: it is only the mutant or recombinant that provide opportunities for rapidly obtaining resistant populations. In confers the ability to survive that proliferates. these cases, in the process of selection for resistance there may be a Although pesticide resistance in insects may not be precisely the severe genetic bottleneck, and special breeding methodologies will be same as resistanceto diseases caused by biologicalorganisms, theremay required to introgress the resistant genes into commercial populations. be some interesting parallels in the evolution and genetics of resistance. Fjalestad et al. (1993) suggest that in the fish farming environment, When chemical pesticides were first developed, insect populations in resistance to a given pathogen will normally develop slowly. However, the field were frequently faced with, from their point of view, a resistance to serious pathogens may develop through natural selection catastrophic situation in which only resistant animals could survive. The in aquaculture populations where the animals have continuously been frequency of resistant genes was extremely low, but nevertheless exposed to the pathogen foronly a few generations, as in the case of TSV resistant individuals and populations eventually emerged. In the field, in P. vann amei (Gitterle, 1999), and with the QX disease in the Sydney where applications were sufficiently intense to cause massive mortal- rock oyster Saccostrea glomerata (Nell and Hand, 2003). In shrimp, ities, single gene resistance normally developed (Roush and McKenzie, which has only recently been bred in captivity, most of the genes that 1987). In studies of the development of resistance in laboratory control resistance will probably have come from the original native populations, where the initial populations were much smaller and populations, although theirfrequency mayhavebeen radicallyaltered as dosage was often reduced so as to increasethe frequency of survivors to populations encountered vastly different conditions. 10–20%, polygenic resistance was the norm (Roush and McKenzie, 1987). In most animal breeding programmes the genetic variation to be This strongly suggests that in a selection programme, the selection exploited is assumed to be that which exists in the base populations protocol itself maywell affect thetype of resistancethat is encountered: when the organisms are domesticated. Nevertheless, over several selection procedures with a limited range of genetic variation and generations with continuous selection pressure on populations of dosages or inoculum pressure that ensure more survivors are likely to prolific species, mutations probably play an important role: this view lead to uncovering and selection for polygenic resistance, whereas is supported by the Iowa corn experiments (Dudley and Lambert, 2004) 5 J . C oc k et al . / A qu ac u ltu r e 28 6 (20 09 ) 1 – 1 1 and much of the work on fruit ies (Harshman and Hoffmann, 2000). In were unimportant in the wild may occur in wild populations, but the the case of shrimps, with extremely large populations and a relatively frequency of resistance may be extremely low. In the case of some new short reproductive cycle, mutations may play a significant role in diseases, previous selection for resistance to another disease may providing genetic variation which can be utilized. In the case of insect confer a level of resistance. This would suggest that in shrimps, even if resistance to pesticides the estimates vary widely from one favourable new diseases attack them in their new intensive cultivation habitats, disease resistance may well exist. This would appear to be especially gene in 102 to one in 101 3 individuals (Mazel and Davies, 1999). The likely in shrimps as the resistance response is not specifictoa favourable mutation rate estimated for E. coli was 4 × 10- 9 per generation (Imhof and Schlotterer, 2001; Foster, 2004). Current particular causal agent. At the same time in these cases the frequency estimates suggest a surprisingly constant mutation rate for a wide of resistant genes is likely to be extremely low. From a breeding point of view the HIV and Hoja Blanca cases are intriguing: If one were to range of organisms of approximately 10- 5 mutations per locus per generation with less than 2% of these being favourable (Frankham et al., search for HIV resistance sources in native Africans, the population 2002; Drake, 1991). The percentage of favourable mutations is probable where the disease first infected human beings, the chances of finding less when they have a large effect than when they have a smaller effect it would be extremely low. Similarly, in Hoja Blanca the resistance (Imhof and Schlotterer, 2001). However, the proportion of favourable or camefrom Japonica rice which was not even grown in the neo-tropics. advantageous mutations would seem to be high in the case of immune- What is certain is that in such cases it is necessary to screen large system genes (Hurst and Smith, 1999). We suggest aconservative figure numbers of individuals from a wide range of populations. Gemmill and Read (1998) suggest that there is a major possibility of 1% of favourable mutationsthat, coupled with amutation rate of 10- 5 , that resistance correlates negatively with other important fitness gives an estimateof 10- 7 favourablemutations perlocus per generation. If we then assume that resistance to a particular diseaseis controlled by components. Consequently, resistance genes could be subject to genes on ten loci, or could occur due to a mutation on any one of ten loci, antagonistic selective forces, which conspire to impose an equilibrium then there willbe onefavourable mutation for every million individuals. frequency somewhere short of complete fixation. There has been much debate about the cost of genetic resistance, but until recently there has In a pond of 10ha (105 m2) stocked at 50 animals m- 2 there are 5million animals, which translates into five favourable mutations. In the case of been little evidence to substantiate this notion (Coustau et al., 2000; favourable mutations that could possibly provide single gene resistance Brown, 2003). Heil and Baldwin (2002) suggested, for plants, that there there are, to our knowledge, no published estimates of the probabilities arevarious possible tradeoffs between fitness and resistance. These can of encountering such genes in large populations. Nevertheless, the very be adapted to the situation in animals, with trade offs being due to rough estimates of favourable mutation rates suggest that they may (a) allocation of fitness limiting resources to resistance traits (b) consti- occur with sufficiently high frequency in shrimp cultivation for them to tutive costs of inducible resistance related to detection pathways and be asignificant sourceof genetic variation fordisease resistanceorother reserves for response (c) auto-toxicity costs in which resistance con- traits. Certainly the opportunity should not be ignored in species where ferring traits are directly toxic or detrimental to the host (d) ecological it is a relatively simple matter to screen millions of animals. costs related to the interaction between the host and the environment: In native or commercial populations, in order for there to be a For example less aggressive cannibalistic feeders might avoid infection selection advantage for disease resistance genes, the disease must be by not consuming moribund infected animals of the same species, but present in the populations. However, little is known about the incidence would also be less fit in situations were feed is limiting and (e) incom- and severityof diseases of Penaeid shrimps in the wild. It is quite possible patibility of resistance to one disease with another. In addition theremay that diseases that are of little orno importancein thenative populations be close genetic linkages between the genes that control disease in theirnativehabitats only become epidemic in theintensive conditions resistance and genes that negatively effect fitness. Heil and Baldwin of cultivated shrimp. Three of the major diseases of shrimp, Taura (2002) indicatethat thereis increasing evidence in plants for tradeoffsin Syndrome Virus (TSV), Yellow Head Virus (YHV) and White Spot fitness related to resistancein the absence of disease pressure. Tian et al. Syndrome Virus (WSSV) were not reported in native populations before (2003) in an elegant piece of work showed a large cost of resistance to the massive epidemics in cultivated shrimp and hence little was known bacterial infection in the quintessential laboratory plant, Arabadopsis about the likelihood of encountering genetic resistance. In the case of (Brown, 2003). Similarly, Kraaijeveld and Godfray (1997) showed a WSSVgenetic analysis indicates that it is arepresentative of a previously strong trade off between the capacity for melanoid encapsulation of unknown virus group now provisionally designated as a whispovirus parasitoids in Drosophila fruit ies and their competitiveness. Gemmill (VanHultenetal.,2000). Nevertheless in both TSV and WSSV genetic and Read (1998) give furtherexamples of tradeoffs for moths with virus differences in resistance have been detected (Gitterle, 1999; White et al., resistanceand mosquitoes for resistance to protozoan parasites. Coustau 2002; Zarain-Herzberg and Ascencio-Valle, 2001). et al. (2000) note that in the case of animal resistance to parasites, In the case of species that apparently have not previously been although the precise physiological mechanisms involved in resistance infected by a particular organism it is not unusual to find resistance. are poorly documented, most of the evolutionary literature is based on Indica rice, originally from Asia, is attacked by the Hoja Blancavirus in the central assumption of a costly investment in defence functions, the Americas, but after screening thousands of varieties, simply leading to a trade off between resistance and other fitness related traits. inherited, dominant resistance was found at a very low frequency in Along the same lines, based on his experience, Detilleux (2001), when germplasm originating in Asia in Japonica type rice (Ou and Jennings, reviewing genetic improvement of livestock, concluded that increased 1969). Similarly, humans have only recently been exposed to HIV and selection pressure to improve commercially important traits is often yet genetic resistance has already been identified related to poly- accompanied by an increase in disease problems, suggesting a trade off morphism on the CCR5 allele. The resistant allele’s prevalence varies between disease tolerance and other desirable characteristics. In the by ethnicity, being as high as 4–15% in Caucasians, and virtually absent case of crustaceans our work in P. vannamei shows a negative genetic in native Africans and East Asians (O’Brien and Moore, 2000). This correlation between resistance to White Spot Syndrome Virus and resistance differs from that of simians that do not develop AIDS growth (Gitterle et al., 2005) and we have repeatedly observed poor (Stebbing et al., 2004) and hence does not seem to have been reproductive fitness of putatively resistant individuals. maintained at a low level after a previous pandemic. Current thinking Recently plant breeders have been moving to more subtle suggests that the CCR5 allele might have conferred selective advan- approaches that include enhancing Induced Systemic Resistance and tage in Caucasian populations under conditions where smallpox was Systemic Acquired Resistance (SAR) in which the plant defences are prevalent (Galvani and Slatkin, 2003). preconditioned by prior infection or treatment that results in resistance These two examples, one from the plant kingdom and the other (or tolerance) against subsequent challenge by a pathogen or parasite from animals, indicate that resistance to new diseases or diseases that (Vallad and Goodman, 2004). The conditioned response which only 6 J . Co ck et a l. / A qu ac u l tur e 2 86 (2 00 9) 1– 1 1 occurs in the presence of infection may be obtained with a lower cost populations may decline at the low levels of disease incidence in the than permanently maintaining a resistance mechanism. resistant populations. 4. Breeding for resistance to diseases 4.1. Success and failure As we have suggested earlier, the high cost of developing In practice disease resistance breeding programs are built genetically disease resistant populations makes this approach suitable empirically and two examples illustrate how a breeding program for when the potential damage is severe, there are no other cost effective disease resistance can be established when knowledge is extremely control measures and there is evidence of genetic variation for the limited and consequently uncertainty is great. Furthermore, one desired trait which is not strongly negatively correlated with other example, breeding for WSSV resistance, indicates some of the pitfalls desirable traits. and dangers of working with very little base line information on the Selection for disease resistance is directly related to its effect on genetic variation for resistance. growth and survival: the objective is not disease resistance per se but rather the impact that disease resistance will have on the desired 4.1.1. Taura Syndrome Virus resistance performance characteristics of theselected stock. Diseases can directly In the mid 1990s theshrimp industry in Ecuador and Colombia was effect both growth and survival. Diseases such as TSV and WSSV cause decimated by TSV. At that time most ponds were stocked with larva severe damage through mortality, although animals that survive may caught in their native habitats or from broodstock captured in the have reduced growth rates. Other diseases such as NHP and vibrio, wild. Pond survivals declined dramatically (Fig. 1) and nobody knew may cause high mortality under some conditions, whilst in others why. There was no doubt of theeconomic importance of thelosses: if a their main effect may beto reduce growth. Up to the present, the main solution was not found to the problem the shrimp industry would focus in selection for disease resistance in shrimps has been to simply disappear. Attempts to control the epidemic by modifying improve survival in the face of epidemics of diseases such as TSV, management practices were largely unsuccessful. In spite of almost which may cause mortalities of 70% or greater and WSSV with total ignorance on the cause of the problem at that time it was noted mortalities close to 100%. We suggest that this emphasis on survival that 20–30% of animals survived and various leaders, technicians and will continue, firstly due to the importance of this trait per se and researchers (including one of us) of the sector surmised that the secondly due to methodological difficulties in screening and selecting survivors could simply be escapes or, on the other hand, they could be for tolerance that allows infected animals to grow well. Furthermore, genetically resistant animals. With little to lose and much to gain, one if selection for growth is carried out under commercial conditions, and of the major producers in Colombia, C.I. Oceanos S.A. initiated a chronic diseases that effect growth rate are endemic, selection for program to select the survivors from infected ponds and use them as growth will effectively be for growth and survival (˜ yield) in the parents for the next generation in a simple, extremely low cost mass presence of the disease. It is noteworthy that this approach is selection scheme. Although the sector was aware of the potential extremely difficult to implement in programmes based on Specific problems of inbreeding, the scheme was deemed acceptable as it Pathogen Free breeding stocks. would rapidly indicate whether there was useful genetic variance for In certain populations a sufficiently high level of disease resistance resistance. Within two to three generations commercial pond survival may be reached to reduce the disease to the level of no longer being rates had once again reached their previous levels indicating the problematic. This has already happened in some shrimp populations success of this simple process (Fig. 1). In later years the industry selected for Taura resistance. However, a watching brief must be kept changed from a mass selection procedure to a combined family and on such diseases as the causal agent may co-evolve with the resistant within-family selection scheme, which incorporated resistant animals stock and become a problem, or the level of resistance in the into the population and monitored levels of Taura to ensure that, with Fig . 1 . Su rv i val o f s h ri m p i n c o m m erc i a l po n d s i n th e Atl an ti c Co as t of Co l om b i a ( re d sq u ar es r efer to s to c ki n g d en s it y). T SV fi rs t ap pe ar ed i n 19 95 . (Fo r i n ter p ret ati o n o f th e re fere n c es to c o l o ur i n t h is fi g ur e l eg en d , th e r ea de r i s re fer red to th e w eb v er si o n of t hi s ar ti c l e. ) 7 J . C oc k et al . / A qu ac u ltu r e 28 6 (20 09 ) 1 – 1 1 the low incidence of the disease under commercial conditions, survival was treated as abinary trait and subjected to a cross-sectional resistance was not lost. linear model with one record per individual. The binary survival data The Taura case indicates several important aspects of deciding for individual animals were recorded when the overall survival rate in whether to include a particular disease resistance trait into a selective the challenge test was approximately 50%, which is the failure rate breeding program and how it can be incorporated. In the case of Taura expected to maximize the accuracy of the linear model. We suggest there was no doubt about the economic importance of the disease, and that looking at the 50% survival in quite small populations, rather than furthermore therewas no known means of controlling or managing the looking for the rare animal that could survive until maturity, will likely disease: when the breeding programme commenced the causal agent uncover polygenic rather than single gene resistance. Thirdly there is had not even been identified. At the same time the simple field negative genetic correlation between growth and resistance and we observation of the presence of survivors under commercial conditions strongly suspect that there is a strong negative association with suggested that useful genetic variance for resistance to whatever was resistance and reproductive performance. Up to the present we have causing the disease might exist. Thus, with the undoubted economic noted that it is difficult to get survivors from challenge tests to potential advantages of resistant populations coupled with the compel- reproduce, however, othershave apparentlybeen ableto obtain progeny ling, but not rigorous evidence for genetic variance in resistance, the from survivors. Nevertheless, in both themass selection programme run decision was taken to set up an extremely simple program to see by a commercial shrimp farm and the family selection program there is whether the supposed genetic variance in resistance could be usefully conclusive evidencethat resistance levels can be improved by both mass deployed. The selection process successfully identified truly resistant selection and family selection and that resistance is lost if selection is individuals; demonstrated that there was indeed useful genetic variance based largely on growth which is negatively correlated with WSSV for resistance; and developed protocols for selection that identified (CENIACUA unpublished data). Nevertheless, the levels of resistance commercially useful resistance. The whole industry moved towards achieved so far are not sufficient to revive the shrimp industry in areas closed cycle mass selection for survival in the presence of TSV and where WSSV is endemic and severe. growth. A hidden factor that probably contributed to the success of the The White Spot case highlights the importance of having a broad Taura resistant selection program was the fact that the populations in genetic base so as to identify sources of resistance: the frequency of the sector were based on wild populations that probably had a broad resistance genes appears to be very low and there may be sources of genetic base, thus increasing the probability of encountering resistance. resistancethat are not included in theinitial populations. In addition it Nowadays we know that the heritability for resistance to TSV is rather highlights the difficulties encountered when there is a negative high for a viral disease, with published estimates in the range 0.20–0.30 correlation between two or more desired traits. We suspect that due (Fjalestad et al., 1997; Argue et al., 2002; CENIACUA unpublished data). to a negative relationship between both growth and reproductive Argue et al. (2002) also found a negative relationship between growth capacity and WSSV resistance some of the most resistant material has and TSV resistance aftera singleround of selection and Mosset al. (2005) been lost from the gene pools used for breeding for resistance. reported a weak but statistically significant negative correlation (r= Furthermore WSSV shows the necessity of selection procedures that -0.15) between mean familyharvest weight and mean familysurvivalin can identifyresistance that will manifest itself at thecommercial level. aTSV challenge test. In other populations selected for resistance to TSV, the growth rate of animals that survived infection was equal to that of 4.2. Selection procedures animals from uninfected tanks when the effects of mortality on population density and its effect on growth were taken into account Selection procedures are needed that ensure that selected stock will (CENIACUA unpublished data). Similarly, in long term studies resistance perform well commercially: this normally means the ability to survive to Tauradoes not appearto be strongly negatively correlated with other an epidemic. Presently selection for disease resistance in designed desirable traits such as general pond survival, growth and reproductive breeding schemes is normally carried out based on survival recorded in fitness (CENIACUA and AKVAFORSK unpublished data). controlled challenge tests. Moss et al. (2005) point out the difficulties of This latter is of particular importance in mass selection, as any developing challenge tests that provide useful information for develop- reduction of selection pressure for disease resistance, if it were ing populations resistant to specific pathogens under commercial negatively correlated with growth, would then lead to increased conditions. Their design should be such that they (i) emulate a natural susceptibility in the population as a whole. Furthermore, although outbreak in theponds and (ii) evaluateallthedefence mechanismof the there islittleconcrete data, thereis considerablecircumstantial evidence shrimps. In order to emulatea natural pond outbreak in achallenge test, that inbreeding depression was minimal in the populations used. it is necessary to identifythenaturalinfection pathways ofthedisease so as to establish an infection protocol that closely mimics them. Selection 4.1.2. Searching for resistance to White Spot Syndrome Virus procedures depend on the natureof the diseaseand thereis no standard The Taura case contrasts with that of breeding for WSSV resistance protocolthat can berecommended for shrimp diseases in general. Anew and indicates some of the potential pitfalls of breeding for resistance protocol is required for each disease. The experience with Taura, in with limited knowledge about the genetic structure of the target several breeding programmes, indicates that effective protocols can be resistance trait. Similar reasoning was used to attempt to rapidly developed and used within on going breeding programmes. Techniques obtain resistant materials using mass selection on commercial farms such as marker assisted selection are postulated as useful; nevertheless and also to incorporateresistance in nuclear stocks of afamilyselection they can only be deployed when protocols have been established to breeding program. However, in this case successful deployment of detect resistant individuals or populations, and closely linked markers commercially viable stock has been an elusive goal. Once again there identified. In the particular case of resistance that increases survival of was no doubt about the economic importance of control. The first sign animals in thepresenceof adisease in an extremely prolific species such of difficulties was the extremely low frequency of survivors, with as shrimps, with a relatively short growth cycle, looking for marker mortalities as high as 98% in the field and in challenge tests. This genes may provide little advantage. It is after all very simple to infect suggested an extremely low frequencyof resistance genes in the initial large numbers of animals and simple select the survivors. populations. Second, was the difficulty of developing a reliable means Breeders tend to look for selection protocols which are simple and of testing for resistance. In commercial mass selection, the selection that maximize heritability and genetic variance. Whilst breeding for pressure depended on the water temperature, which varied from year survival in the face of WSSV, the time to 50% survival in animals to year and in the family selection the controlled challengetests did not inoculated with WSSV, was chosen for reasons given before. The levels appear to select truly resistant materials (Gitterle et al., 2005). of resistance in selected populations, as measured by both 50% Following the classical method for analyzing challenge test data, survival and final survival, were both increased but survival of 8 J . Co ck et a l. / A qu ac u l tur e 2 86 (2 00 9) 1– 1 1 resistant stock has still not reached the levels required for commercial diseases. Unfortunately, several of the mass selection programmes that use of the stock. have been carried out by commercial operations producing their own In the particular case of breeding for survival, recently developed stock have not been welldocumented. Mass selection in the absenceof a longitudinal models (e.g. proportional hazards and survival score particulardisease maylead to low levels of resistance and devastation by models) that utilize information from the full course of the challenge that particular diseasewhen it is introduced. On the other hand there is test have provided greater selection accuracy than conventional cross- some evidence that inbreeding with mass selection for such traits as sectional models (Gitterle et al., 2006; Ødegård et al., 2006, 2007). These growth and pond survival may not always lead to serious problems in longitudinal models facilitate analysis of time-until-death and survival breeding programmes. This view is supported datafrom theP. vannamei within sub-periods, but, for maximum accuracy, require the challenge programme at the Oceanic Institute from which Moss et al. (2007) test to proceed until all animals are dead or mortality levels off. conclude that under favourable conditions inbreeding effects are Fjalestad (2005) pointed out that disease resistance is a candidate statistically significant but small for growth, and are minimal for for theuse of indirect selection protocols in fish due to the difficulty of grow-out survival, in the absence of viralpathogens. Whilst the negative measuring traits such as survival on individuals. It opens the way for effects of inbreeding on survival and growth are small under favourable combined between and within-familyselection. Furthermore, indirect conditions they increase when animals grow in poor environments selection is particularly appropriate when the desired character is (Doyle et al., 2006; Moss et al., 2007). Furthermore, through selection difficult to measure precisely (Fjalestad 2005). However, for indirect substantial gains for growth can likely be achieved at low to moderate selection for survival to compete with direct selection the correlation levels of inbreeding (Moss et al., 2007). De Donato et al. (2005) followed between the correlated trait and survival must be high. This suggests 11 generations of mass selected lines in Venezuela and reported that when breeding for increased survival it is important to ensure increased resistance to endemic diseases such as IHHNV and no signs that the selection protocols, whatever the breeding methodology, of deterioration on thefitness-related traits. In the caseof shrimpsunder truly identify the desired trait and provide the opportunity to reach commercial conditionsa 20% mortalityin the grow-out period and a50% levels of resistance that are commercially useful. mortality in the phase from spawning to stocking ponds are considered normal and accepted. This translates into a survival rate of only 40% 4.3. Breeding methodologies which would be unacceptablein manyspecies. We surmise that there is little build up of deleterious genes in shrimp populations mass selected The advantages and disadvantages of different breeding meth- for pond survival and growth under commercial conditions; those odologies can be found in the standard texts on animal breeding. In animals that carry deleterious genes will be eliminated naturally as this section the advantages and disadvantages of different breeding animals that carry them neither survive nor grow well. This type of self methodologies are discussed solely with respect to the specific case of elimination of poor types is readily achie ved in highly prolificspecies disease resistance. Mass selection, family selection and combined grown under commercial conditions where a moderate loss of unfit family and within-family selection can all be effectively used in animals is the norm. On the other hand inbreeding moderately to selective breeding for disease resistance depending on the circum- severely affects survival in the presence of TSV and WSSV (Moss et al., stances. Family based designs are particularly effective for those traits 2007). Similarly the Venezuelan populations described by De Donato where heritability is low and hence the information on the individual et al. (2005) when confronted with TSV, after manycycles of selection in breeding candidate’s own record provides little information on its the absence of the virus, proved to behighlysusceptible. Thus control of additive genetic capacity. It seems likely that family selection will also inbreeding is particularly important when improving such traits such as be particularly appropriate for resistance under polygenic control disease resistance, nevertheless, it is probably prudent for breeding where the heritability is likely to be intermediate or low. On the other programs to manageinbreeding irrespectiveof the traits underselection hand, if disease resistance is under the control of few genes or is (Moss et al., 2007). monogenic, and also of extremely low frequency simple mass The experiences with TSV highlight some of dangers of loss of selection may be effective but also implies a risk of greatly reduced heterozygosity due to inbreeding in the absenceof aparticular pathogen. overall genetic variability in the population. Special breeding metho- Themass selected Venezuelan populations (De Donato et al., 2005)were dologies such as backcrossing may be expedient so as to introgress free of TSV for many generations, but when TSV appeared the levels of resistancewere extremely low. Similarly, the SPF Konapopulations from resistance into populations with other desirable characteristics and to maintain genetic variability. the Oceanic Institute from Hawaii, that were not selected for TSV Family selection has several advantages over mass and individual resistance proved to be extremely susceptible to TSV (Srisuvan et al., selection when developing disease resistant populations. For many 2006). Breeding programmes that maintain their breeding nuclei as reasons it may be advantageous to maintain the nuclear breeding Specific Pathogen Free populations run the risk of producing animals stock free of diseases and several programmes are based on Specific that are extremely susceptible to those specific pathogens unless Pathogen Free breeding nuclei. Amongst the most important is to selection for resistance is incorporated into the breeding scheme: this provide good quality stock that is not loaded with diseases for becomes complex when there are several pathogens on the list. dissemination to commercial producers. With mass selection the only Mass selection is not as effective as family selection when possible manner of obtaining information to select future breeders is simultaneously selecting for traits that are negatively correlated, a by challenging them and this almost inevitably means exposing them case which appears to be quite common for disease resistance. On the to the disease followed by complex procedures to eliminate the other hand, family selection for improved resistance is currently based disease. In some cases it may be possible to select for resistance to on sib-testing without exposing the breeding candidates to the toxins produced by pathogens or use Marker Assisted Selection and pathogen, which only utilizes the 50% of the additive genetic variance hence no exposure to the live pathogen is necessary. On the other accounted for by the between-family component. It is evident that hand, with family selection, close relatives (usually full- and half-sibs) development of appropriatetesting and biosecuritymeasures that make of the breeding candidates can be challenged with disease organisms it possible to safely introduce animals surviving the challenge test (or and the information generated from these tests used to rank the non- gametes from survivors) willsubstantially increase the efficacy of family exposed breeding candidates. based selection schemes targeting resistance to diseases. There is no A further problem with mass selection when dealing with extremely individual selection if challenge tests are carried out on separate virulent diseases such as WSSV is the rapid narrowing of the genetic populations that are not included in the breeding nucleus. In contrast, variation in the population, which will restrict future genetic improve- mass selection is particularly effectivewhen the desired trait determines ment and may make populations extremely vulnerable to other whether an individual survives, when no resistance has yet been 9 J . C oc k et al . / A qu ac u ltu r e 28 6 (20 09 ) 1 – 1 1 detected or when frequencies of the desired trait are extremely low and extremely virulent and kill their host before having the opportunity to large numbers of animals from different genetic backgrounds need to be infect a new host, as is the case for example with Ebola virus, are often screened. We suggest that in thesesituations mass selection can be used not able to maintain themselves (Ebert, 1998)). Selection pressure in to screen massive numbers of individuals, literally millions, and to select these cases is initially for less virulence in the pathogen, as has been those rare individuals that are able to survive a severe disease epidemic shown to occur in myxomatosis although over the long term a series of and go on to produce. In these cases it is necessary to ensure that the strains of differing virulence coexist (Aparicio et al., 2004). Conversely challenge test used re ects commercialconditions and that theselection when host resistance levels are increased in a population the pathogen pressure is maintained: if there is a cost to the resistance then will tend to evolve mechanisms that overcome that resistance. Recently populations are likely to revert rapidly if the selection pressure is various strains of TSV have been recognized with varying levels of relaxed. With the extremely heavy selection pressure applied in such virulence (Srisuvan et al., 2006). Fortunately it appears that shrimp cases the disease resistant animals finally encountered may lack many populations resistant to one particular strain are also resistant to other other desirable traits for commercial production. strains (Moss et al., 2005; Srisuvan et al., 2006), that is to say thereis not In plants it is quite common to detect diseaseresistancein extremely astrain by resistant genotypeinteraction. In Colombia there are notable poor plant types. In order to remedy this situation plant breeders differences in the sequences in the CP2 section of TSV samples taken in introgress disease resistance from unimproved or wild species into 1998 and in 2006/7, indicating evolution of the virus strains (CENIACUA improved populations using backcrossing techniques. We suggest that unpublished data). It is not yet clear as to whether this evolution is this approach may be appropriate for shrimps. In those cases where related to increased virulence in the face of shrimp populations bred for there is not a ready source of commercially useful resistance in the resistance to TSV. Nevertheless, breeders should take into account both current commercial or nuclear breeding stock populations, it may be the co-evolution of host resistance and pathogen virulence and the possible to produce millions of larvae or juveniles and screen these for possible lack of selection pressurefor diseases by constantlymonitoring survival using mass selection. If resistant types are discovered, and we levels of resistance, even for diseases that have ceased to be a problem. have no way of knowing beforehand the probability, then the resistant Furthermore, it may bepossibleto guard against loss of resistance by the animal or animals can then be used to introgress resistance into the host or evolution of more virulent pathogens by a well designed commercial populations. Various techniques such as backcrossing may dissemination programme in which mass selection forendemic diseases be used to introgress the desired genes and eliminate the undesirable is included as part of the process for multiplication of broodstock. genetic load associated with them in the initial resistant genotype. The search for the rare individual that survives in the case of 4.4. Base populations and population size catastrophic diseases is dangerous as there is no guarantee of the durabilityof theresistance. Forseveral decadesplant breeders havebeen Selective breeding programmes are only appropriate when genetic using pyramiding of genes to lower the probability of break down of variation exists for the traits to be selected. A number of breeding resistance(Pink, 2002; Pederson and Leath,1988). In this process several programs in fish may havefailed dueto low genetic variation in the base single genes that provide resistance are“pyramided”into the population population (Teichert-Coddington and Smitherman, 1988; Huang and so that all individuals carry more than one gene-for-gene resistance Liao, 1990). Miles and Pandey (2004) indicate that plant improvement gene. This reduces the probability of breakdown enormously. For program tend to make more rapid progress after the introduction of more diverse germplasm. Similarly, in cassava the success of modern example if the probability of breakdown is one in 10- 8 of the pathogen overcoming either of two resistances in a given individual in a given breeding efforts has been attributed to the great genetic variability which the modern programmes acquired from the outset (Kawano and period of time it willbe reduced to one in 10- 16 if two genes are present. In order to pyramid genes it is necessary to identify the sources of Cock, 2005). On the other hand, in the long term divergent selection for resistance in resistant individuals. Until recently this was extremely oil and protein content of maize in Illinois starting from an extremely difficult to achieve: nowadays with molecular markers it may be narrow genetic base, Dudley and Lambert (2004) state tha t “10 0 possible to identify different sources of single gene resistance on generations of selection have not eliminated genetic variability and an different loci and to determine which resistant genes an individual upper limit has not been reached.” In several long term selection trials possesses. Hence, use of single gene resistance should preferably be for body weight in mice with effective population sizes of less than 100 based on more than one source of single gene resistance pyramided some, but not all, populations have reached a plateau (Hill and Bunger, into the population with marker assisted selection to ensure that 2004). In reviews of long term selection in laboratory and domestic selected resistant phenotypes are also pyramided genotypes. animals much of the initial gains areattributed to thegenetic variancein Breeding for resistance is a continuous dynamic process: the genetic the initial base population, and later response to mutations in the composition of both pathogen and host are continually changing (Ebert, population (Hill and Bunger, 2004; Weber, 2004). 19 98 ). Carius et al. (2001) found significant genetic variation among In manyanimal improvement programmes the breeding design pays clones of the freshwater crustacean Daphnia magna for susceptibility to careful attention to maintaining genetic variation, but less attention is its parasite Pasteuria ramosa and significant genetic variation among paid to ensuring maximum diversity in theinitial foundation stock. Part isolates of the bacterial parasite P. ramosa for infectivity to it host of the reason is undoubtedly related to the fact that most domesticated D. magna. Loss of resistance in a population can be the result of changes specieshave been selected for alongperiod of timefor specific traits and in the host and the genetic make up of the pathogen. After host the introduction of more genetic diversity to a foundation population resistance has been developed above a certain level in a population, would undoubtedly introduce many undesirable traits. Breeders simply disease incidence may be reduced to extremely low levels. Under these cannot use native stocks to enhancetheiralready improved stocks as the conditions selection pressure is reduced for resistance, and if there is a native populations are so far behind in performance that they are not fitness cost associated with the resistance this will be lost. We suggest competitive (Hill and Bunger, 2004) and could, at least in the short term that in shrimp populations, with prolific breeders, the drift towards induce negative genetic gain in the desired traits. In the case of Penaeid susceptibility is potentially rapid. This viewpoint is supported by our shrimps this is not currently a major problem as the existing improved observations of a combined family and within family selection populations are mostly only a few generations from the wild popula- programme for resistance to TSV in which populations not subjected tions. However, as populations are improved it willrapidly become more to continuous selection pressure for resistance appeared to lose difficult to incorporate genetic diversity and still maintain the genetic resistance (CENIACUA unpublished data). gains in desired traits. Furthermore, in many countries importation of Pathogen populations are continually evolving and adapting to the wild populations or specific populations is restricted due to biosecurity host environment which is itself changing. Pathogens which are measures. In addition the introduction of new germplasm into breeding 10 J . Co ck et a l. / A qu ac u l tur e 2 86 (2 00 9) 1– 1 1 programme with Specific Pathogen Free nuclei is onerous and time Eb er t, D. , 1 99 8 . E xp er i m en tal ev ol u ti o n of p ar as i tes . S c i en c e 2 82 , 14 32 – 14 35 . Fj al es ta d, K. T. , 20 0 5. In : G j ed re m, T . (E d. ), S el ec ti o n M et h od s . I n S el ec ti o n a nd B re ed in g consuming. Thus the relatively new shrimp breeding programs should Pr og ra ms i n Aqu ac u l tu r e. Sp ri n ge r, N et he rl an d s , p p . 159 – 171. make every effort to obtain genetically diverse populations before the Fj al es ta d, K.T. , Gj e dr em , T ., G j er de , B ., 19 93 . G en eti c i m p ro vem e nt o f d is e as e re si s ta nc e populations have diverged substantially fromthe wild populations from i n fi s h : an o ver vi ew . Aq ua c ul t ur e 111, 65 – 74. Fj al es ta d, K. T. , Gj ed r em , T., C ar r, W .H ., S wee n ey, J .N ., 19 9 7. Fi na l R ep o rt: T h e S h ri m p which they were recently derived. Br ee di n g Pr og ra m, Se le c ti ve Br ee di n g of P ena eus va nn am ei . T h e Oc e an i c I n st i tu te, Unfortunately, studies on how the basepopulation should be formed Wai m an al o , H I , U SA. (i.e. the numberof individuals to besampled from one orseveral founder Fl ege l , T.W ., Al d ay -S an z, V., 19 9 8. T h e c ri s i s i n A si an s h ri m p aq u ac u l tu re : c u r re n t s t atu s an d f ut ur e n ee ds . J . Ap p l . I c h th yo l . 1 4, 26 9 –2 73 . strains, their mixing, and the intensity of selection to be applied during Fl egel , T. W., N i el se n, L., T h amav it , V., Ko n gti m , S., Pas h araw ip as , T. , 20 0 4. Pre sen c e o f the initial generations) their effects on the magnitude and va riability of mu l ti pl e vi ru se s i n n on -d i s eas ed, c ul ti vat ed sh ri m p at h ar ves t. Aq u acu l tu re 24 0, 55 –6 8. the long term selection response and inbreeding are few (Holtsmark Fos te r, P.L ., 2 00 4 . Ad apt i ve m ut ati o n i n Es c her i c hi a c ol i. J . B ac te ri o l . 18 6 (15 ), 4 8 46 – 48 5 2. et al., 2006). Fra nk h am , R ., B al l ou , J . D., B r i sc o e, D .A. , 2 00 2 . I nt ro d uc t i on t o C on s er vat io n G en et i cs . Ca m br i dg e Un i v ers i ty Pr es s , U K. 6 17 p p . In the case of shrimp breeding for diseaseresistanceit would appear Gal v an i, A. P., Sl at ki n , M ., 20 0 3 . E val u at in g p l agu e an d sm a ll p o x a s hi s to ri c a l se l ec ti ve that in order todetect genetic resistance in existing populations a wide a pr es s u re s fo r t h e C CR 5 – de l ta 3 2 H I V- re s is t an c e al l el e. Pr o c . N atl . A c ad . Sc i . U. S . A. range of origins of base populations should be explored and screened. 10 0, 1 52 76 –1 52 7 9. Gem m i l l , A.W ., R ead , A. F., 199 8 . Co u n ti n g th e c os t of di s ea se r es i s tan c e. T ren d s E c ol . Furthermore, large populations (millions of animals) should be Ev ol . 13 , 8 – 9. produced and screened to detect mutants or recombinants that confer Gi tt erl e , T., 199 9 . Ev al u ac i ón de l a re si s ten c i a d e d i fer en t es p ob l ac i o ne s d el c a ma ró n resistanceto catastrophic diseases. Anydesirable traits obtained in these m ari n o L it op ena eus va nn am ei (B oo n e 19 31 ) a l Vi ru s d el Sí n d ro m e d el Tau r a (T SV) baj o c o n d ic i o n es c o n tr ol ad as . Th e si s . Un i ve rs i d ad J o rg e T ad eo Lo zan o , B o go ta, massive screening efforts should then be incorporated into the base Co l om b i a, 7 4 p p . population and maintained irrespective of the breeding scheme being Gi tt erl e , T ., Sa lt e, R ., Gj e rd e, B ., C o c k, J ., J o h an s en , H. , Sal aza r, M ., Lo zan o , C . , Ry e, M ., used. 20 0 5. Gen et i c ( c o)v ar ia ti on i n r es i s tan c e to w hi t e sp o t sy n dr o me v i ru s ( WS SV) an d h arv es t w ei gh t i n Pen aeu s (L i top ena eus ) va nn am ei . Aq u ac u l tu re 2 4 6, 1 39 –1 49 . Gi tte rl e, T., Ød eg ård , J ., Gj er de , B ., R ye , M ., Sa lte , R . , 2 0 06 . Gen et ic pa ram ete rs an d ac c u rac y 5. Conclusions of s el ec ti o n fo r r es is ta nc e to Wh i te S po t Sy nd r om e Vi ru s (WS SV) i n P ena eus (L ito pen aeu s) van na me i u s i ng d i ffer en t s ta ti st ic al m od el s . Aqu ac u lt ur e 251, 210 –21 8. Goy ard , E ., Pat ro is , J ., Pe i gn on , J ., Van aa, V. , Du fou r, R ., Vi al l on , J ., B ed ie r, E. , 20 0 2. Sel ec t io n Selective breeding provides a useful means of controlling shrimp for b ette r g ro wth of P ena eu s s tyli ro str i s i n Ta hi ti a nd New C al ed on i a. Aqu ac u l tur e 2 0 4, diseases when these currently cause severe losses, other control 46 1– 46 8. measures are difficult, useful genetic variation in resistance exists and Ha rs h m an , L .G ., Ho ffm an n , A .A. , 2 0 0 0. Lab o rat or y s e le c ti on exp er i m en ts u s in g Dr os o- ph i la : wh at do th ey re al ly tel l u s ? Tr ee 1 5, 32 – 36 . resistance is not negatively and stronglyassociated with other desirable He i l, M . , B al dw i n , I .T. , 20 0 2. F it n es s c o st s o f i n d uc e d r es i st an c e: em er gi n g ex pe ri m en t al traits. Genetic variation in resistance may be encountered either in the su p p or t fo r a s l i p p ery c on c ep t. Tr en d s P l an t S c i. 7, 6 1– 6 7. initial base populations or may spontaneously arise due to mutations or He n ni g , O. L., A rc e, S .M . , Mo s s , S.M . , Pa nt oj a, C . R ., Li g ht n er, D .V. , 20 0 5 . Dev el o pm e nt o f a new recombinants. Effective protocols are required to detect resistance; sp e c ifi c p at ho g en fre e p op u l ati o n o f th e Ch i n es e e sh y p r awn , Fenn ero pen aeu s c hi n ens i s P ar t I I . Se c on d . Q ua r. A qu ac . 2 5 0, 57 9 –5 8 5. due to the prolificacy of shrimps large populations can be screened so as Hi l l , A. V.S ., 2 0 01. T h e gen o m i c s an d g en et ic s of h u ma n i n fec t io u s d i s eas e s u sc e pt i bi l i ty. to identify sources of resistancethat occur at low frequencies. The most An n u. R ev. G en o m. Hu m . G en et . 2 , 3 73 –4 0 0 . appropriate breedingmethodology dependson thenature of the disease Hi l l , W .G ., B u n ger , L. , 2 00 4 . 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