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Abstract

Interspecific hybridization is a route for transgenes from genetically modified (GM) animals to invade wild populations, yet the ecological effects and potential risks that may emerge from such hybridization are unknown. Through experimental crosses, we demonstrate transmission of a growth hormone transgene via hybridization between a candidate for commercial aquaculture production, GM Atlantic salmon (
Salmo salar) and closely related wild brown trout (
Salmo trutta). Transgenic hybrids were viable and grew more rapidly than transgenic salmon and other non-transgenic crosses in hatchery-like conditions. In stream mesocosms designed to more closely emulate natural conditions, transgenic hybrids appeared to express competitive dominance and suppressed the growth of transgenic and non-transgenic (wild-type) salmon by 82 and 54 per cent, respectively. To the best of our knowledge, this is the first demonstration of environmental impacts of hybridization between a GM animal and a closely related species. These results provide empirical evidence of the first steps towards introgression of foreign transgenes into the genomes of new species and contribute to the growing evidence that transgenic animals have complex and context-specific interactions with wild populations. We suggest that interspecific hybridization be explicitly considered when assessing the environmental consequences should transgenic animals escape to nature.    

1. Introduction

The production of genetically modified (GM) plants and animals has prompted considerable debate surrounding the environmental and ecological consequences should they escape [1,2]. The majority of research has assessed the performance of such organisms and their potential interactions with conspecifics and other species under experimental conditions [3–6]. In both plants and animals, the potential ecological risks are modulated by the reproductive capabilities of the transgenic organism, the fitness effects of the transgene and the potential for interbreeding with wild conspecifics. Parallel with these risks is that of introgression into gene pools of closely related species, especially between species that hybridize naturally [7]. Natural hybridization rates of wild, non-transgenic organisms are facilitated by reductions in reproductive barriers associated with mating behaviour; this has been observed in the translocations and invasions of species [8,9], including following release or escape of strains that have been exposed to domestication selection [10–12]. Successful artificial transgenic hybridization between two species of loach (genus
Misgurnus) has been reported, yet these species are not known to hybridize naturally [13]. In contrast to plants [14], the potential ecological consequences of interspecific hybridization involving transgenic animals are unknown.

Atlantic salmon (
Salmo salar), a candidate for growth-enhancing transgenic biotechnology for commercial production, hybridizes naturally with closely related brown trout (
Salmo trutta). Natural levels of hybridization rarely exceed 1 per cent [15], yet translocations, as well as escapes and introductions of domesticated salmon [16–18], can increase rates to as much as 41 per cent [17]. Hybridization between Atlantic salmon and brown trout is asymmetric, where the maternal origin of the hybrids varies among regions. The maternal species is predominately salmon within the natural geographical range of sympatry, while it is trout in areas where the species have come into secondary contact ([19] and references therein). Despite such regional differences, mortality prior to exogenous feeding is higher among hybrid offspring of trout mothers relative to hybrids with salmon mothers [19,20]. Given these biological patterns, we hypothesized that the transgene may further affect the outcome of hybridization, especially in terms of hybrid viability and hybrid growth rates.

Here we test the potential for transgene exchange through interspecific hybridization between transgenic Atlantic salmon and brown trout and whether this would generate novel ecological interactions. To do so, we created a series of experimental crosses and reared the offspring in both hatchery-like conditions and contained stream mesocosms designed to more closely emulate nature. These crosses and subsequent rearing experiments were designed to test: (i) whether the transgene can be transmitted into hybrid offspring via artificial mating; (ii) the survival of hybrid offspring; (iii) the phenotypic expression of the transgene in hybrids, particularly in relation to that observed in transgenic salmon; and (iv) the effect of direction of hybridization (i.e. whether the mother was a salmon or a trout) on phenotypic expression of the transgene. We used salmon hemizygous for the transgene, which enabled us to compare full sibling transgenic and non-transgenic hybrids (i.e. largely control for parental and other non-random genetic effects). Subsequently, to investigate potential ecological consequences of such hybridization, we undertook a replicated experiment to (v) quantify the effects of the presence of transgenic hybrids (from both maternal origins) on the growth of non-transgenic (henceforth referred to as wild-type) and transgenic salmon in stream mesocosms under food-limited conditions.