An overview of methods for measuring enhanced fitness and invasiveness, their environmental consequences and how they can be applied in Environmental Risk Assessment

Hooftman, Danny. 2010 An overview of methods for measuring enhanced fitness and invasiveness, their environmental consequences and how they can be applied in Environmental Risk Assessment. [Keynote] In: 11th International Symposium on the Biosafety of Genetically Modified Organisms, Buenos Aires, 15-20 November 2010. (Unpublished)

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In this talk I will highlight various experiments and modelling efforts for testing the possibilities for escape, persistence and invasiveness of transgenes. I do not pretend to give a definitive answer on the question which methods should be used for conducting Environmental Risk Assessment (ERA) for abiotic stress transgenes. Though as an awareness session, I would like to overview several fitness interactions between environment and plants causing potential invasiveness that have been experimentally studied and modelled over the last 10 years. Various overview studies have been published providing wider results and questions, which can provide further guidance (Ellstrand 2003; Andow & Zwahlen 2006; Chapman & Burke 2006; Chandler & Dunwell 2008). A compilation of such studies will provide a checklist of identified potential hazards which could be falsified using experimental data and model based explorations in time and space. It is such approach which is promoted in the proposed new EFSA guidance document on ERA of genetically modified plants (EFSA 2010). The framework I am using here is based on this guidance, leading through a hierarchical set of questions which I group into the following: (i) indications within biological information of the species itself and it wild relatives for invasiveness (ii) potential persistence of the transgene in plants under agricultural conditions; (iii) potential persistence of the transgene outside the agricultural environment in ferals and (iv) potential persistence of the transgene outside the agricultural environment in closely related species. Using biological information: asking whether a GM plant can grow and reproduce under current conditions and whether it can hybridize with sympatric plants (relatives or native ferals). This asks for basic but full life-cycle information about the species, reproduction and survival ability, both above and below ground (Hails & Morley 2005). Certainly the outcrossing pathway has been well described for many species (Ellstrand 2003; Armstrong et al. 2005). Hence the ability crops and wild relatives to hybridize is now generally accepted for most major crops and has been found even over long distances up to 21 km (Watrud et al. 2004; Reichman et al. 2006). However, this still could mean that de ERA for invasiveness could not potentially stop here: in the EU, corn has no wild relatives, which could make a difference in ERA in comparison to e.g., Northern America. Testing for persistence of the transgene in plants under agricultural conditions, i.e., volunteers and gene flow to other crops. Studies such as Warwick et al. (2008) and D’Hertefeldt et al. (2008) found transgenic plants to persist for several generations in agricultural fields. Simulation models as Genesys (Colbach et al. 2001) show that in systems including various crops, planted in rotations, such volunteers could persist and potentially spread through a whole area within 10s of years (see also Claessen et al. 2005; Hooftman 2006). Even when volunteer populations do not become weedy, they could act as a genetic bridge between different cultivars and towards wild relatives (Hall et al. 2000; Reagon & Snow 2006). Transgenes have been found to persist for several years in and around agricultural fields through storage in volunteers and feral crop plants (Pessel et al. 2001; Pivard et al. 2008), potentially presenting such a hazard on a larger temporal scale. Appropriate estimation of the risks involved will vary much dependent on the quality of the life-cycle data available, in which it is important to gather all life-cycle data from repeated single experiments under non-optimal conditions (Hails & Morley 2005). Next to these simulation approaches, a wide range of population models has been developed over the last years, both matrix and integral models, which can be very useful for modelling population persistence: some examples are Bullock (1999); Thompson et al. (2003); Hall et al. (2006); Allainguillaume et al. (2006); Hooftman et al. (2007) and Damgaard & Kjaer (2009). The main question for volunteers to answer seems whether and how much populations decrease in the other crops in the years between growing the GM crop of interest. Persistence of the transgene outside the agricultural environment. For feral populations, second generation transgenes, like biotic stress tolerance, could differ fundamentally from first generation transgenes. The stress situation likely exists outside the field as well, whereas e.g., an herbicide tolerance is less likely to provide an advantage unless the herbicide is present. However, the non-agricultural environments are likely much more diverse than within agricultural fields, making controlled-environment studies (greenhouse and lab) less applicable. Field-based studies seem necessary here to a range of conditions to test for environment x genotype interactions (Mercer et al. 2006; Ridley & Ellstrand 2009). Garnier & Lecomte (2006a; 2006b) developed a further set of matrix approaches that can be used, next to the ones mentioned above. Potential persistence of the transgene outside the agricultural environment in closely related species. Few studies have shown a direct relationship of transgenes with fitness in early hybrid generations (e.g., Snow et al. 2003). More likely, the initial persistence of the transgene depends strongly on processes surrounding plant fitness, which are transgene related. However, certainly with transgenes for tolerance for abiotic stress, the transgene is likely to be part of a, limited, package of genes which could provide a fitness advantage over time. So any test for differences between transgenic and non-transgenic races likely has to follow the same methods as most studies done on non-GM crops. Fitness analyses and the long-term persistence of such hybrids has been studied to a large extent in species such as Lactuca (Hooftman et al., 2005; 2007), Brassica (Allainguillaume et al. 2006; Jorgensen et al. 2009), Helianthus (Reagon & Snow 2006; Rieseberg et al. 2003; 2007) and Raphanus (Snow et al. 2001; 2010; Campbell et al. 2006; 2009; Ridley & Ellstrand 2009). A wide variety of population models as mentioned above is available for analyses. However, fitness analyses are far from straightforward in hybrids in terms of experiments. Recent studies by Campbell et al. (2009) and Hooftman et al. (2010) have shown that experiments should take multiple generations under selective conditions, since sorting among genotypes could lead to better performance than assumed on early generation hybrids only. This can have clear effects on the population structure and the total presence of the transgene in populations, certainly under a relative invariable selection pressure as an adverse abiotic stress will provide (Hooftman et al. 2008). Also the competive ability of hybrids compared to the parental species might be altered (Hauser et al. 2003; Vacher et al. 2004) or even differ under varying levels of stress (Mercer et al. 2007). Recently genetic hitchhiking and position of transgenes on the genome have gained increasing attention (see Uwimana et al. in this session). Furthermore, recent evidence in Brassica points to large scale difference in introgression rate and fitness of hybrids between mitochondrial and nuclear DNA fragments (Allainguillaume et al. 2009). In conclusion, all the experimental evidence on both transgenic and non-transgenic crop systems indicates that an integrative approach asking a hierarchical range of ecological questions is needed. Assuming the phenotypic change, caused by the transgene in the crop, will be similar in plants after escape is often proved plainly wrong. Many methods exist to get a better understanding. Abiotic stress presents certainly new challenges in environments and interactions to deal with, since it could provide substantial niche shifts of plant species. Regulators, industry and other stakeholders will have to decide how to acknowledge those interactions between environments, the transgene and plant biology in general. In this we will have to realize that GM plants might present other risks than their conventional counterparts or present new hazards not provided by such counterparts. References: Allainguillaume et al. (2006) Molecular Ecology, 15: 1175-1184. Allainguillaume et al. (2009) New Phytologist, 183: 1201-1211. Armstrong et al. (2005) Molecular Ecology, 14: 2111-2132. Andow & Zwahlen (2006) Ecology Letters, 9: 196-214. Bullock (1999) Aspects of Applied Biology, 53: 205-212. Campbell et al. (2006) Ecology Letters, 9: 1198-1209. Campbell et al. (2009) Evolutionary Applications, 2: 172-186. Chandler & Dunwell (2008) Critical Reviews in Plant Sciences, 27: 25-49. Chapman & Burke (2006) New Phytologist, 170: 429-443. Claessen et al. (2005) OIKOS, 110: 20-29. Colbach et al. (2001) Agriculture, Ecosystems and Environment, 83: 235–253. Damgaard & Kjaer (2009) Journal of Applied Ecology, 46: 1073-1079. D’Hertefeldt et al. (2008) Biological Letters, 4: 314-317. EFSA (2010). Guidance on the environmental risk assessment of genetically modified plants (draft version) Ellstrand (2003) John Hopkins University Press, Baltimore. Garnier & Lecomte (2006a) Ecological Modelling, 194: 141-149. Garnier & Lecomte (2006b) Ecological Modelling, 197: 373-382. Hails & Morley (2005) Trends in Ecology and Evolution, 20: 245-252. Hall et al. (2000) Weed Science, 48: 688–694. Hall et al. (2006) Proceedings of the Royal Society B, 273: 1385-1389. Hauser et al. (2003) American Journal of Botany, 90: 571-578. Hooftman et al. (2005) Journal of Applied Ecology, 42: 1086-1095. Hooftman (2006) 9th International Symposium on Biosafety of GMOs, Jeju Island, Korea. Hooftman et al. (2007) Journal of Applied Ecology, 44: 1035-1045. Hooftman et al. (2008) Journal of Applied Ecology, 45, 1094-1103. Hooftman et al. (2010) Environmental Biosafety Research, in press. Jorgensen et al. (2009) Environmental Science and Pollution Research, 16: 389-395. Mercer et al. (2006) Evolution, 60: 2044-2055. Mercer et al. (2007) Ecology Letters, 10: 383-393. Pessel et al. (2001) Theoretical and Applied Genetics, 102: 841-846. Pivard et al. (2008) Journal of Applied Ecology, 45: 476-485 Reagon & Snow (2006) American Journal of Botany, 93: 127-133. Reichman et al. (2006) Molecular Ecology, 15: 4243-4255. Ridley & Ellstrand (2009) Biological Invasions, 11: 2251-2264. Rieseberg et al. (2003) Science, 301: 1211-1216. Rieseberg et al. (2007) Genetica, 129: 149-165. Snow et al. (2003) Ecological Applications, 13: 279-286. Snow et al. (2010) New Phytologist, 186: 537-548. Thompson et al. (2003) Ecological Modelling, 162: 199-209. Vacher et al. (2004) Theoretical and Applied Genetics, 109: 806-814. Warwick et al. (2008) Molecular Ecology, 17: 1387-1395. Watrud et al. (2004) PNAS 101: 14533-14538.

Item Type: Publication - Conference Item (Keynote)
Programmes: CEH Topics & Objectives 2009 - 2012 > Biodiversity
UKCEH and CEH Sections/Science Areas: Hails
NORA Subject Terms: Ecology and Environment
Agriculture and Soil Science
Date made live: 11 Sep 2013 14:21 +0 (UTC)

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