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The Proposed Release of the Yellow Fever Mosquito, Aedes Aegypti Containing a Naturally Occurring Strain of Wolbachia Pipientis

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The Proposed Release of the Yellow Fever Mosquito, Aedes Aegypti Containing a Naturally Occurring Strain of Wolbachia Pipientis J. Verbr. Lebensm. Journal fu¨ r Verbraucherschutz und Lebensmittelsicherheit DOI 10.1007/s00003-011-0671-x Journal of Consumer Protection and Food Safety CONFERENCE PROCEEDINGS ‘‘DECISION MAKING AND SCIENCE’’ The proposed release of the yellow fever mosquito, Aedes aegypti containing a naturally occurring strain of Wolbachia pipientis, a question of regulatory responsibility Paul J. De Barro • Brendan Murphy • Cassie C. Jansen • Justine Murray Ó CSIRO (2011) published by Springer Basel AG 2011 Abstract In 2010 a proposal to release the yellow regulatory frameworks. An acceptable regulatory fever mosquito, Aedes aegypti, containing an intra- solution has been found, but the novelty of the sci- cellular symbiotic bacterium, Wolbachia, as a means ence is such that the appropriateness of the of reducing the severity of outbreaks of dengue fever regulatory process now needs to be reviewed to was lodged in Australia. The mosquito was infected ensure that it is no more onerous for both the pro- with Wolbachia through embryonic microinjection. ponents and the regulators than it needs to be. This proposal uncovered a gap in the regulatory process normally used to assess the release of species Keywords Biological control Á Dengue Á into Australia. Firstly, while the association between Arboviruses Á Genetically modified organism Á the mosquito and the bacterium was new, both spe- Legislation Á Wolbachia Á Aedes aegypti Á cies naturally occurred in Australia and so legislation Risk assessment governing the introduction of new species into Aus- tralia was ruled not relevant. Secondly, the infection of the mosquito with Wolbachia did not involve gene technology and so was not subject to legislation 1 Introduction governing the approval of genetically modified organisms. The solution came through the decision The introduction of species into a country is usually a to use existing legislation to regulate Wolbachia as a regulated process. However, there are instances veterinary chemical product. This was a good out- where the release request falls outside normal regu- come as it overcame the barrier that a lack of latory pathways. In such instances, the proponent is regulatory oversight may have posed to field trials placed in a regulatory ‘no man’s land’. One response taking place. Furthermore, the approach taken could be to simply go ahead with the release, but this demonstrated a very high level of scrutiny with leaves the proponent vulnerable should the intro- regard to biosafety. This case is an example of how duction lead to adverse consequences. On the other science is leading to advances that outstrip existing hand, they can attempt to cobble together a ‘work around’ that enables regulators to bring the request under their jurisdiction. An example is the 2009/2010 Conference Proceedings ‘‘Decision Making and Science—the request to release into Australia a mosquito that had Balancing of Risk Based Decisions that Influence Sustainability been infected with a symbiotic bacterium, Wolbachia of Agricultural Production’’ 7th and 8th October 2010 in Berlin, Germany. Sponsored by the OECD Co-operative Research pipientis, as a means of reducing the incidence of Programme. dengue fever. The complication was that both the mosquito and the Wolbachia used occur naturally in & P. J. De Barro ( ) Á B. Murphy Á C. C. Jansen Á J. Murray Australia, but not as a mosquito containing the bac- CSIRO Ecosystem Science, EcoSciences Precinct, PO Box 2583, Brisbane 4001, Australia terium. The challenge was to find a regulatory e-mail: [email protected] process that could assess the release proposal. 123 P. J. De Barro et al. 1.1 Background reproductive output of female insects that do not carry Wolbachia if they mate with a Wolbachia The Eliminate Dengue Program (http://www. infected male (Hoffmann and Turelli 1988). In addi- eliminatedengue.com/en/HOME.aspx) is a large multi- tion to CI, Wolbachia in A. aegypti greatly reduces the institution research program involving Australia, replication of dengue and other human pathogens in Thailand, Vietnam and the USA and is led by the the mosquito (Kambris et al. 2009; Moreira et al. University of Queensland. It aims to control mosquito- 2009; Bian et al. 2010). Wolbachia can also shorten borne diseases such as dengue, yellow fever and the lifespan of A. aegypti (McMeniman et al. 2009) Chikungunya. and causes a ‘bendy proboscis’ phenomenon in Dengue fever and its more extreme form dengue ageing A. aegypti females whereby they cannot haemorrhagic fever are major global human health penetrate human skin for blood feeding (Turley et al. problems estimated to cause between 50–100 million 2009). cases annually (http://www.who.int/mediacentre/ factsheets/fs117/en/). Both the geographic spread and 1.2 Horizontal transfer severity of outbreaks are increasing. In Australia, the vector, Aedes aegypti, occurs in the northern parts of Wolbachia is known to transfer between unrelated the country (Russell et al. 2009). Dengue is not species in a process known as horizontal transfer, but endemic in Australia but is continually reintroduced this is a seemingly rare event and the mechanism is by means of infected travellers (Gould and Solomon unknown. Experimental attempts to achieve hori- 2008). As in other parts of the world, outbreaks in zontal transfer have been largely unsuccessful (Heath Australia are becoming more frequent. The most et al. 1999; Huigens et al. 2004). This poses the recent occurred in 2009 in Cairns and resulted in interesting question of how Wolbachia establishes in over 1,000 reported cases (Anonymous 2009a, b). insect hosts naturally when it is so hard to establish Currently, there is no cure or vaccine for dengue and infections in the laboratory. This has been a central control is targeted at reducing vector abundance. question for the Wolbachia research community for The Eliminate Dengue Program is using the natu- many years and despite considerable effort, the rally occurring obligate intracellular insect mechanisms of natural transfer remain unknown. bacterium Wolbachia pipientis to suppress transmis- The only two recorded examples of natural horizon- sion of dengue viruses (Moreira et al. 2009). Insects tal transfer have been between different parasitoids are naturally infected with a range of intracellular superinfecting the same insect host (Heath et al. bacteria such as Wolbachia. These bacteria are not 1999; Huigens et al. 2004). It should also be noted transmitted infectiously between individuals, but are that the scientific community researching Wolbachia instead transmitted vertically, from mother to off- is quite large and there is a significant body of liter- spring, through the eggs of an infected female. ature on Wolbachia biology, with over 1,500 peer Wolbachia are extremely common, infecting more reviewed papers published. Currently, approximately than 20 % of all insect species (Werren et al. 1995; two scientific papers on Wolbachia are being pub- Jeyaprakash and Hoy 2000; Hilgenboecker et al. lished every week—so there is a considerable 2008). Currently, Wolbachia does not naturally infect appreciation of the biology and natural history of A. aegypti although there is evidence to suggest that Wolbachia. The general consensus of the scientific in the past it may once have been infected (Klasson community is that natural horizontal transfer events et al. 2009, Woolfit et al. 2009). The Wolbachia used are extremely rare. However, the wide distribution of to infect A. aegypti was isolated from Drosophila Wolbachia among insects is explained by the many melanogaster. It is known as wMel and is present in millions of years that Wolbachia is believed to have numerous species of Diptera in Australia. Aedes been associated with insects, which has allowed time aegypti was infected via microinjection into mosquito for numerous rare events to accumulate. eggs (McMeniman et al. 2009). Subsequently, all eggs produced by infected females contain Wolbachia. 1.3 Production of Wolbachia-infected Aedes Wolbachia can confer a range of beneficial, neutral aegypti and pathogenic phenotypic characteristics on hosts (McGraw and O’Neill 2004), including cytoplasmic The process by which Wolbachia was successfully incompatibility (CI). This reproductive trait provides a transferred to A. aegypti was complex. Wolbachia are mechanism by which Wolbachia is able to invade an routinely cultured in insect cell lines (Dobson et al. interbreeding insect population by reducing the 2002; Furukawa et al. 2008; Jin et al. 2009; O’Neill 123 Risk assessment of Wolbachia pipientis and Aedes aegypti in Australia et al. 1997; Xi and Dobson 2005) and the principal Biodiversity Conservation Acts; it does have respon- means of transfer to novel hosts is by microinjection, sibility under the Gene Technology Act. which is both technically challenging and unpre- dictable in terms of success (McMeniman et al. 2008). 2.1 Biological control agent The key to the successful transfer was believed to be due to the pre-adaptation of Wolbachia in mosquito Initially it was thought that wA. aegypti could be cell cultures of Aedes species. Here, the wMel strain considered an inoculatively released biological con- used to infect A. aegypti was maintained in an trol agent, one where the agent is released in small A. albopictus cell line for *240 passages (about numbers, establishes, increases in numbers and then 2.5 years) before being transferred to an A. aegypti spreads of its own accord. While Australia has spe- cell line and cultured for another 60 passages. Sub- cific legislation governing the introduction and sequent genomic analysis of this strain after serial release of biological control agents, the Biological passages revealed a number of genetic changes that Control Act 1984, in most cases this legislation is not occurred in the Wolbachia genome. It is believed that used. The reason is that the legislation deals pri- the genetic changes incurred during cell culture marily with a specific situation, one where there are were critical elements of the adaptation process conflicting interests regarding whether the release required for successful transfer.
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