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GENIMPACT SYMPOSIUM Bergen, 2 – 4 July 2007 Genetic engineering in aquaculture: possibilities and limitations possibilities and limitations Lorenzo Colombo Department of Biology University of Padova, Italy [email protected] Trying to be good Transgenesis into the germinal line of fish is a consolidated technology displaying significant achievements, like 2-11-fold growth rate enhancement by fish-GH-gene transfer (autotransgenesis) in more than 30 teleosts, mostly of aquaculture interest. GH-transgenic fish need less time, water and energy to reach market size and convert food more into protein and less into fat. Food safety issues for consumers are presently deemed to be negligible, as GH-transgenic fish are substantially equivalent to nontransgenics. Private companies have invested for the mass culture of transgenic fish (mainly salmon). According to FAO, fast-growing fish may help to meet future animal protein demand. On the brink of extinction ? Why the cultivation of transgenic crops, which are mainly allotransgenic, have conquered 100 million hectares since 1997 and are presently expanding globally at 10% per year, while the commercial farming of fast-growing GH-transgenic fish is not yet allowed and viewed with widespread skepticism ? Is the opposition against the mass cultivation of transgenic fish based on sound science, traditional culture or mass mediainfluenced attitude ? Are transgenic fish an example of reckless manipulation of life and, hence, doomed to extinction, or the result of inadequate application of otherwise useful technology ? BIODIVERSITY BIOREPERTOIRE Evolutionary mechanisms Evolution by natural selection and speciation Metaevolution by domestication and genetic improvement Selective parameters Fitness (reproductive success) Performance (production or service capacity) Agents Natural forces Biological interactions Reproduction control Reproduction manipulation Courses Unplanned and undirected No design Planned and directed Intelligent design Percent of total species domesticated 1 Time (years before present) Land versus water. Most land species were domesticated earlier than aquatic species but, in the past 100 years, many more aquatic species than land species have been domesticated. Duarte et al. (2007), Science, 316, 382-383. Global pace of species domestication Species groups Time since domestication (years before present) Number of 50% species species domesticated domesticated 90% species domesticated Land plants 250 4000 2000 Land animals 44 5000 146 Freshwater animals 180 22 4 430 Marine animals 250 19 4 Marine Plants 19 32 <10 Duarte et al. (2007), Science, 316, 382-383. Traditional domestication process Domesticated biodiversity Development of rearing practices providing shelter, food, care and assisted reproduction in exchange for confinement and terminal sacrifice. Broodstock open to exchanges with wild-type genetics. Domesticated biorepertoire Application of selective breeding, either empirically or according to quantitative genetics to improve progeny performance. Broodstock belonging to a selected race or line. Sale of progeny without further royalties. Production improvement in aquaculture Genetically holistic approaches Selective breeding Sequential genetic gains Interspecific hybridization Single genetic gain Polyploidization Single genetic gain Integrated expression of novel allele combinations Integrated expression of combined heterospecific genomes Integrated expression of high-ploidy (>2) genomes Recommended management of genetic resources Biodiversity Biorepertoire Gene flow Wild populations Farmed stocks Evolution by natural selection Domestication by genetic improvement Biotechnological approaches in aquaculture Genetically reductionistic approaches Gene transfer into the germinal line DNA vaccination Transgene with perpetuated transmission and expression Plasmids with indipendent and transient expression The third phase of domestication Transformed biorepertoire Application of gene transfer technology to jump start a trait of interest without progressing through small genetic gains along multiple generations. Broodstock belonging to a stabilized transgenic line. Right to patent and license a transgenic line. Possible monopolistic control of the product market. Risk of transgenic crossbreeding. contamination of wild-life by A big leap for mankind Application of gene transfer technology in agriculture marked a transition from domesticated biorepertoire to transformed biorepertoire, while in fish culture it would be a leap from domesticated biodiversity to transformed biorepertoire. For this transfer, two main safety issues must be satisfied: Nutritional equivalence: when food transgenic components are identical or comparable to those of traditional food. Ecosystemic compatibility assessed by: fitness estimate: probability that population be established in the wild; a transgenic dynamic impact estimate: level of harm imposed on recipient biocommunities; genetic impact estimate: probability of transgenic contamination of feral conspecifics. How transgenic crops got their way Nutritional equivalence: not given for granted because of the prevalent transfer of transgenes from other taxa (allotransgenesis); consumers’ safety issue resolved pragmatically. Ecosystemic compatibility: debated as an affair internal to agriculture rather than biodiversity because: the genetic interface with isospecific wild plants is minimized due to their absence, rarefaction or genetic incompatibility with polyploid genomes of cultured plants; fear of possible cross-contamination with conventionally or organically cultivated crops; supposed cross-contamination with agricultural weeds. Why GH-transgenic fish flopped Public perplexity because growth-enhanced GH-transgenic fish would be the first animal product for human consumption to be genetically engineered. Nutritional equivalence: generally conceded for GHtransgenic fish because integration of autotransgenes, like fish-GH-transgenes, should not alter qualitatively the host transcriptomic and proteomic profiles, at least not in a way to represent a health hazard for consumers. Ecosystemic compatibility: strongly contested to safeguard biodiversity because: due to the recent domestication process of a great number of aquatic species, the genetic interface with wildlife is vast and still permeable in both directions. Transgenic contamination Although gene transfer between fish species can occur naturally, as in introgressive hybridization, transgene trade with wild fish is not be equivalent to the passage of native genes, because transgenes are products of intelligent design and patentable. The hazard of transgenic contamination of feral conspecifics is double-faced: if they are indigenous, it represents a contamination of biodiversity; if they are naturalized from alien escapees, it may entail exacerbation of non-genetic impacts on other species, but not a loss of genetic integrity in truly natural biodiversity. Entering the wrong way Since transgene insertion in wild genomes may be irreversible, ecosystemic risk assessment based on field tests is the currently obligatory step for approving applications for the mass culture of possibly fertile transgenic fish. This precautionary measure determined a deadlock because: fish tested in natural ecosystems are essentially unrecoverable; tests in secluded environments are of limited significance and can provide only circumstantial estimates with limited predictive capacity. Hence, endless moratoria have been the only outcome. An industrial miscalculation To overcome the impasse, the only option is to solve the problem about how to maintain the fertility of confined spawners to perpetuate a transgenic line, while securing complete reproductive sterility in transgenic fish for grow-out Surprisingly, private companies interested in developing transgenic fish culture for commercial purposes have not promptly realized that complete sterility of marketed transgenic fish was a top priority also for them because it is required: to safeguard aquatic wildlife; to ensure full market control on their product; to avoid being sued at later times for unforeseen transgenic contaminations. Coolest inventions 2003 No more sex Apparently, the rush in the implementation of gene transfer in agriculture instigated the belief that this was also possible in fish culture. To remedy this misconception, triploidy induction by pressure or heat shocks was proposed to secure sterility, but this claim was soon dismissed for lack of consistent 100% efficiency, while fish have high reproductive capacity and may escape in large numbers from culture facilities. Among the options at hand, the simplest is the double sterility approach where triploidy induction is combined with other techniques to fill up the gap in its per cent effectiveness, such as allotriploidization of infertile interspecific hybrids. Let’s make it better Whatever the best sterilizing solution, it would be deplorable to dump gene transfer technology as inapplicable to fish culture, just because the first attempts were inadequate. In the past, geneticists have made wonders by platonically gazing at the shadows of genes as reflected in the realized phenotypes. Now, in the era of genomics, we have the privilege of admiring life in full shining in order to responsibly take care of our growing needs. Given the fact that the human population is presently increasing at the rate of half billion people every 6 years, transgenic fish may provide a convenient source of cheap animal protein from non-carnivorous species in countries most afflicted by heavy demographic pressure. A bomb in the alcove 1650 : 0,5 billion people + 0,5 BL / 150 years 1800 : 1 billion + 1 BL / 130 years 1930 : 2 billion + 1 BL / 30 years 1960 : 3 billion + 1 BL / 15 years 1975 : 4 billion + 1 BL / 12 years 1987 : 5 billion + 230.000 / day Present increment rate: + 7 milioni / month + 84 milioni / year Picture above x 170.000 + 1 BL / 12 years 1999 : 6 billion + 0,5 BL / 6 years 2005 : 6,5 billion