Genome-edited livestock: Ethics and social acceptance

The agricultural application of genetic engineering has advanced in the field of crop breeding. In 1994, the US Food and Drug Administration (FDA) approved a genetically modified (GM) tomato variety, the world’s first GM crop for food consumption (Bruening and Lyons, 2000). In this GM tomato (the Flavr Savr), ripening was delayed by the insertion of an antisense gene that interferes with polygalacturonase production. Although the regulatory approval of GM crops largely demands strict assessments of the environmental risks and food safety, the commercial cultivation of GM crops with an exogenous gene (termed transgene) has spread to at least 28 countries, including the USA, Brazil, Argentina, India, Canada, China, and some European countries (Ishii and Araki, 2016). Conversely, there have been few regulatory approvals regarding GM livestock, with the exception of GM goats for “pharming” in which biopharmaceuticals are manufactured using transgenesis (FDA, 2009). Currently, older genetic engineering practices, such as transgenesis, are giving way to genome editing. Genome editing tools, such as zincfinger nucleases (ZFNs; Klug, 2010), transcription activator-like effector nucleases (TALENs; Joung and Sander, 2013), and the clustered regularly interspaced short palindromic repeat (CRISPR)/Cas 9 (Barrangou and Doudna, 2016), can break DNA double strands at target sites and then achieve various types of genetic modification via non-homologous end-joining (NHEJ) or homology-directed repair (HDR), thus potentially adding new value to agriculture (Figure 1). Recent reviews suggest that NHEJ is preferred in crop genome editing because the resultant plants are considered to contain no transgenes, which is one of the major concerns over GM crops from regulatory and social aspects (Hartung and Schiemann, 2014; Voytas and Gao, 2014; Araki and Ishii, 2015). Genome editing has also been applied in livestock breeding (Carlson et al., 2012; Hai et al., 2014; Crispo et al., 2015; Cui et al., 2015; Proudfoot et al., 2015; Wang et al., 2015a; Wang et al., 2015b; Wang et al., 2015c; Carlson et al., 2016; Fischer et al., 2016; Oishi et al., 2016; Petersen et al., 2016; Tanihara et al., 2016; Wang et al., 2016; Whitworth et al., 2016). Animals modified via NHEJ are unlikely to impose substantial risks on the environment because they can be managed within a farm, unlike GM crops, which are intentionally released into the environment (field cultivation). Thus, one can presume that the products derived from genome-edited livestock will soon be accepted in society if the food safety can be confirmed. However, it would be inappropriate to presume that such a favorable course of events is the only possibility. In November 2015, the FDA approved a GM salmon for food consumption (FDA, 2015). Nonetheless, citizen groups and environmentalists still loudly oppose the FDA’s decision about its safety. In addition, they questioned the environmental risk that it posed to wild salmon populations; despite that the sterile GM fish is only raised in landlocked tanks (Pollack, 2015). Such public movements may have prolonged the FDA review of the GM salmon. It took nearly a quarter of a century and cost more than $77 million (Van Eenennaam and Muir, 2011). Psychological investigations have suggested that GM animals are viewed as less acceptable than GM plants and that people’s sense of ethics has a more significant effect on the acceptance than other factors such as the perceived risks, the recognized benefits, or the trust in regulators and researchers (Zechendorf, 1994; Siegrist, 2000). Likewise, complex situations are likely to emerge in the case of livestock genome editing because animals modified via NHEJ are also genetically modified. In the present article, we consider the practical and ethical bottlenecks in obtaining the social acceptance of animal breeding by genome editing, focusing on the development of livestock strains.