Gene flow from transgenic maize to landraces in Mexico: An analysis

doi:10.1016/j.agee.2007.05.007

Agriculture, Ecosystems & Environment

Volume 123, Issues 1–3, January 2008, Pages 109-115

https://doi.org/10.1016/j.agee.2007.05.007 Get rights and content

Abstract

A highly publicized study in 2001 reported that maize landraces in Oaxaca, Mexico were found to contain transgenes, yet not all follow-up research has detected transgenes in the same region. Continued testing for transgenes in Mexican maize, and calls for the removal of transgenes from landraces, have only fueled the debate about the dynamics of gene flow from transgenic maize to landraces in Mexico. This paper reviews these recent findings and discusses how evolution may be expected to alter the frequency of transgenes in crop populations over time. Further, it shows that calls for removing transgenes must be interpreted in light of two ecological complexities: (a) it may be impossible to purge a particular gene from a population and (b) scientists’ ability to accurately determine the presence or absence of transgenes is limited by challenges related to sampling. The paper concludes by outlining two ways forward for removing transgenes from landraces.

Introduction

The genetic diversity found in landraces (traditional, open-pollinated varieties) of major crops in centers of origin comprises one of the world's most important natural resources for future plant breeding efforts and global food security (Altieri et al., 1987). Conserving crop diversity with and through the very evolutionary processes that generate variability (Brush, 1989, IPGRI, 1993) leaves landraces open to change via gene flow and introgression. With the advent of genetically engineered crops, this openness to genetic change became a cause for concern among some conservationists.

Maize is arguably the world's most important food crop, with global production of ∼700 million metric tons in 2005, 10% more than wheat and rice (FAOSTAT, 2006). Mexico, the center of origin of maize and the world's fourth largest maize producer (FAOSTAT, 2006) is home to 59 distinct races (Wellhausen et al., 1952, Sanchez et al., 2000). Landrace maize is still grown on >80% of Mexico's maize acreage (Aquino et al., 2001), largely by poor, indigenous farmers in Mexico's rural South and East (Mann, 2004). Many of these landraces are grown only in particular regions, often under low-input conditions. The cultural practices of Mexican farmers, such as seed sharing, mixing of seed, and farmer selection, influence the evolutionary processes acting on these populations (Bellon and Berthaud, 2006).

In 1996, 2 years after NAFTA led to sharp increases in US maize exports to Mexico, many US maize farmers began shifting to genetically modified (GM) maize, causing concern in Mexico about possible effects on local maize. In 1999, the Government of Mexico introduced a de facto moratorium on experimentation with and production of GM maize, but its importation (for consumption, not planting) from the USA continued (CEC, 2004, González Aguirre and Aguilar Muñoz, 2006). In response, ∼150 non-governmental organizations (or NGOs) called for a complete ban on the importation of GM maize in 2000; that same year, the Government signed the Cartagena Protocol on biosafety that mandates adherence to the precautionary principle while making regulatory decisions (González Aguirre and Aguilar Muñoz, 2006). So when Quist and Chapela (2001) published an article in Nature documenting the presence of transgenes in maize landraces in rural Oaxaca, their findings provoked demonstrations and recriminations. Quist and Chapela (2001, p. 542) claimed to find “a high level of gene flow from industrially produced maize towards populations of progenitor landraces”. Their results launched a vigorous debate and spurred several other studies. This paper reviews this body of recent research on transgenes in Mexican maize and their sampling protocols to consider their implications for the conservation of maize landraces. Before turning to the recent studies, a discussion of the dynamics of gene flow and introgression is warranted.

Section snippets

Transgene introgression in agricultural systems

Transgenes can move among crop populations in two ways: through seed exchange and/or cross-pollination among adjacent fields. These represent seed-mediated and pollen-mediated gene flow, respectively. Mexican farmers exchange seed to revitalize their populations or initiate new seed lots (Louette et al., 1997, Rice et al., 1998, Bellon and Risopoulos, 2001). They also occasionally plant seed from DICONSA (a Mexican state institution that distributes subsidized grain), which imported some maize

Are there transgenes in Mexican maize landraces?

At least ten studies have been conducted since 2001 to test for the presence of transgenes in Mexico (see Table 1). The first was that of Quist and Chapela (2001), intended to establish a baseline for landrace genetics prior to the arrival of transgenes in rural Oaxaca (Ezcurra et al., 2001). The authors found that approximately 1% of kernels in all four landrace ears collected from two communities contained transgenes (see Table 1), though their small sample size reduces the strength of this

Potential for reduction of transgene frequency in landrace populations

In response to their unexpected results, Ortiz-García et al. note that common evolutionary forces – gene flow, drift, and selection – “may have prevented [transgenes] from persisting at detectable frequencies in the sampled seed” (Ortiz-García et al., 2005a, p. 12342). They argue that the amount of transgenic seed entering the region (i.e. gene flow) may have declined for two reasons: first, DICONSA ceased importing grain by 2003 (SEDESOL, 2003); second, increased GM awareness may have led

Calls for ‘decontamination’

These scientific studies unfolded in the midst of a roiling political debate. The detection by Quist and Chapela (2001) and the ETC Group (2003a) of transgenes in Mexico's maize landraces evoked strong responses from many farmers and NGOs, who demanded that the Mexican government and international regulatory bodies respond to transgenic ‘contamination’. The CEC was petitioned in 2002 by 21 indigenous groups (supported by more than 90 letters from NGOs) to organize a study on the “impacts of

Potential methods for transgene reduction

Nevertheless, scientists must articulate ways forward and paths to practices that may reduce or remove transgenes from landrace populations. Where there are maize landraces with transgenes in them, two strategies could be employed to decrease (albeit not eliminate) the frequency of transgenes in landrace populations. First, there could be a two-pronged effort to test landrace populations for the presence of transgenes (with methods used by farmers groups in Mexico) and to replace ‘contaminated’

Conclusion

Although the debates over GM agriculture are far from over, they are shifting to a new terrain where the prevailing question is not whether states should allow GM agriculture, but how best to regulate its effects. In this light, difficulties of detecting and reducing transgene introgression underscore the importance of strategies and practices that may prevent transgene introgression from occurring in the first place. The importance of the recommendations outlined by the tri-national CEC

Acknowledgements

K.L.M. thanks the International Institute for Education, COMEXUS, and a Fulbright-García Robles grant for funding her research in Mexico in 2005. J.D.W. conducted research for this paper as a Killam Fellow in the Department of Geography at the University of British Columbia. We thank three anonymous reviewers for their comments on previous versions of the ms. Our paper also benefited from conversations with L. Campbell, K. McSweeney, A. Snow, and especially H. Perales. We are solely responsible

References (47)

M. Bellon et al.
Small-scale farmers expand the benefits of improved maize germplasm: a case study from Chiapas, Mexico
World Devel.
(2001)
E. Rice et al.
Farmers’ use of improved seed selection practices in Mexican maize: evidence and issues from the Sierra de Santa Marta
World Devel.
(1998)
A. Storfer
Gene flow and endangered species translocations: a topic revisited
Biol. Cons.
(1999)
M. Altieri et al.
Peasant agriculture and the conservation of crop and wild plant resources
Conserv. Biol.
(1987)
D.A. Andow
Editorial: Negative and positive data, statistical power, and confidence intervals
Environ. Biosaf. Res.
(2003)
P. Aquino et al.
Selected maize statistics
M. Bellon
The ethnoecology of maize variety management: a case study from Mexico
Hum. Ecol.
(1991)
M. Bellon et al.
Transgenic maize and the evolution of landrace diversity in Mexico: the importance of farmers’ behavior
Plant Physiol.
(2004)
M. Bellon et al.
Traditional Mexican agricultural systems and the potential impacts of transgenic varieties on maize diversity
Agric. Hum. Val.
(2006)
J. Bergelson et al.
Surveying patterns in the cost of resistance in plants
Am. Nat.
(1996)

S. Brush

Rethinking crop genetic resource conservation

Conserv. Biol.

(1989)

CEC (Commission for Environmental Cooperation)

Maize and Biodiversity: The Effects of Transgenic Maize in Mexico

(2004)

CIMMYT (Centro Internacional de Mejoramiento de Maíz y Trigo)

Los últimos escrutinios de maíz criollo en México no revelan la presencia del promotor relacionado con los transgenes

(2002)

D.A. Cleveland et al.

Detecting (trans)gene flow to landraces in centers of crop origin: lessons from the case of maize in Mexico

Environ. Biosaf. Res.

(2005)

N.C. Ellstrand et al.

Population genetic consequences of small population size: implications for plant conservation

Ann. Rev. Ecol. Syst.

(1993)

ETC Group (Action Group on Erosion, Technology and Concentration)

Contamination of Bt Genetically Modified Maize in Mexico Much Worse Than Feared

(2003)

ETC Group (Action Group on Erosion, Technology and Concentration)

Open Letter from International Civil Society Organizations on Transgenic Contamination in the Centers of Origin and Diversity

(2003)

ETC Group (Action Group on Erosion, Technology and Concentration)

Maize Rage in Mexico: GM Maize Contamination in Mexico—2 Years Later

(2003)

E. Ezcurra et al.

Evidence of gene flow from transgenic maize to local varieties in Mexico

FAOSTAT, 2006. http://faostat.fao.org (accessed June 16,...

R.L. González Aguirre et al.

Bioseguridad y actores sociales

IPGRI (International Plant Genetics Resources Institute)

Diversity for Development: The Strategy of the International Plant Genetic Resources Institution

(1993)

N. Kaplinsky et al.

Maize transgene results in Mexico are artifacts

Nature

(2002)

Cited by (54)

Navigating compounding uncertainty: Farmer strategies amid biosecurity crises in western Uganda
2021, Geoforum
Citation Excerpt :
Secondly, geographers have examined the geopolitical implications of the securitization of life (Hinchliffe and Ward, 2014; Lowe, 2015). These works have focused on the increasing militarization and fortification of borders, monitoring, and control over non-human life in an attempt to separate “good” from “bad” life (Collard, 2012; Mansfield, 2011; Mercer and Wainwright, 2008; Sundberg, 2011). The connections between control over life and the policing of boundaries led Braun (2007) to argue that “biosecurity weds biopolitics with geopolitics” (p. 23).
In western Uganda, state biosecurity measures designed for the elimination of uncertainty through monitoring, control, and eradication of plant disease merely offload responsibility for uncertainty, placing it elsewhere, often in the arms of farmers. In this paper, I explore the ways in which uncertainty is operationalized and challenged by farmers in the face of banana Xanthomonas wilt (BXW), a deadly plant disease causing widespread losses across East Africa. Farmers negotiate differing claims to certainty regarding the disease and availability of agricultural extension from multiple actors, often through improvisation and experimentation. These practices highlight how knowledge networks between the state, farmers, and scientists are reshaped due to biosecurity and disease. The findings suggest the potential for a deeper entrenching of inequality as the improvised knowledge networks follow familiar patterns of state investment and social difference. Farmers with the social and economic capital to manage uncertainty are able to do so, while resource-poor farmers face a compounding uncertainty stemming from multiple sources which build on each other. On the other hand, compounding uncertainty may also produce space for strategic alliances between farmers and other actors as it draws multiple concerns together. Overall, these results reflect the importance of attending to the political ecology of knowledge in biosecurity regimes and in environmental governance more broadly.
Wild wheat to productive drylands: Global scientific practice and the agroecological remaking of Palestine
2017, Geoforum
This paper traces how scientific research on wheat (Triticum) worked to establish Palestine as a region sought for colonization. Recent work in geography has refined our understanding of agricultural expansion as an outcome of colonization, however, this work leaves the place-making capacity of agricultural research largely unexplored. My claim is that rather than a byproduct of colonization, wheat research served to remake Palestine as a biophysical region in need of improvement and colonization. I show how a shift in the plant sciences from research in taxonomy to plant breeding corresponded to an agro-climatic shift on Palestine from an undesirable, arid region to a promising dryland agricultural region. In this way, wheat research drew Palestine and the United States into a wider effort to transform arid areas into agricultural drylands. Drawing on a previously unexplored episode of technical cooperation between researchers in the United States and Palestine, I argue that we must examine how wildness, native-ness, and agro-climatic suitability are scientifically constituted within and not apart from colonial conquest. In doing so, the paper calls for reconsideration within geography and political ecology of the place-making relationship between colonization and scientific practice.
Persistence of seeds, seedlings and plants, performance of transgenic wheat in weed communities in the field and effects on fallow weed diversity
2015, Perspectives in Plant Ecology, Evolution and Systematics
Citation Excerpt :
Multiple studies reported unintended contamination of non-GM seed lots due to seed persistence in soil and GM plant volunteering in subsequent conventional crops or along the transport routes (Andersen et al., 2010; Demeke et al., 2006; Friesen et al., 2003; Hecht et al., 2014; Knispel and McLachlan, 2010; Mallory-Smith and Zapiola, 2008; Schafer et al., 2011). Volunteering and outcrossing of transgenic plants with traditional landraces or wild relatives pose a serious agricultural and environmental problem (Joergensen et al., 2009; Holman et al., 2011; Mercer and Wainwright, 2008; Mortensen et al., 2012; Piñeyro-Nelson et al., 2009). In particular, persistence and spread of the transgenes in agroecosystems and changes in weed management practices due to the introduction of herbicide-resistant crops are known to have direct and indirect effects on biodiversity in fallow fields, often leading to the shifts in the species composition of the weed communities, with resistant genotypes dominating (Culpepper, 2006; Green and Owen, 2011; Harker et al., 2005b; Vencill et al., 2012; Warwick et al., 2009).
Introduction of transgenic crops to agriculture has raised concerns about their effects on agro-ecosystems. We compared nine conventional lines of spring wheat with six genetically modified (GM) lines that contained transgenes of resistance against powdery mildew (Pm3b gene) or against fungi in general (Chi and Glu genes). We assessed the persistence and performance of these lines without competition and in experimental weed communities in the field, their seed germination in the laboratory, their survival in fallow plots and effects on post-harvest vegetation in the field.
In competition with weeds, the GM lines showed reduced seed number, plant height and biomass allocation to seeds than their corresponding non-GM lines. No such performance differences were observed without competition. The seedlings of GM lines did not persist longer than those of the corresponding non-GM lines in fallow plots. In the field, GM and non-GM wheat lines had similar performance and persistence and both were able to reproduce in dense weed communities and to survive during winter on fallow plots. Stored in soil in the laboratory, the seeds of GM and non-GM lines either germinated quickly or lost their viability after 3 months. GM and non-GM lines had no differential effects on the structure and diversity of fallow plant communities within the 6-month period of monitoring. Poor seed longevity yet successful plant persistence in weed communities or on fallow plots indicate that not removing a population of growing plants presents a greater risk than allowing the build-up of a soil seed bank regarding the potential escape of transgenic wheat to the environment. Strong varietal differences in persistence point out the importance of case-by-case assessment of new GM varieties and indicate that transgenic traits should preferably be introduced into varieties with low persistence.
Bacterial community structure in maize residue amended soil with contrasting management practices
2015, Applied Soil Ecology
Citation Excerpt :
Since 1991, the ‘International Maize and Wheat Improvement Centre’ (CIMMYT) realizes experiments to compare the traditional agricultural practices with conservation agriculture (Govaerts et al., 2009). In agricultural systems in large parts of the world, especially in Mexico, maize is the main cultivated crop (Mercer and Wainwright, 2008). In rainfed conditions maize is commonly planted on the flat.
Agricultural practices affect the bacterial community structure in soil. It was hypothesized that agricultural practices would also affect the bacteria involved in the degradation of crop residue. Soil was sampled from four different agricultural practices, i.e. conventional agriculture on the flat or on beds, or conservation agriculture on the flat or on beds. Cultivating crops on the flat is done traditionally, but cultivating crops on beds was introduced so as to avoid water logging during the rainy season and its potential negative effect on yields. Soil from these four treatments was amended in the laboratory with maize residue (Zea mays L.) or its neutral detergent fibre (NDF) fraction, mostly consisting of (hemi) cellulose, and incubated aerobically for 14 days. Maize residue was applied to soil as it is left in the field in conservation agriculture and NDF was added to study which bacteria were favoured by application of (hemi) cellulose. Soil was incubated aerobically while the carbon mineralization and the bacterial population were monitored. On the one hand, the relative abundance of phylotypes belonging to bacterial groups that preferred low nutrient environments was higher in soil with conservation agriculture (e.g. Acidobacteria 17.6%, Planctomycetes 1.7% and Verrucomicrobia 1.5%) compared to conventional practices (Acidobacteria 11.8%, Planctomycetes 0.9% and Verrucomicrobia 0.4%). On the other hand, the relative abundance of phylotypes belonging to bacterial groups that preferred nutrient rich environments, such as Actinobacteria, showed an opposite trend. It was 11.9% in conservation agriculture and 16.2% in conventional practices. The relative abundance of Arthrobacter (Actinobacteria) and Bacillales more than doubled when maize residue was applied to soil compared to the unamended soil and that of Actinomycetales when maize or NDF was applied. Application of organic material reduced the relative abundance of a wide range of bacterial groups, e.g. Acidobacteria, Bacteroidetes, Planctomycetes and Verrucomicrobia. It was found that application of organic material favoured the same bacterial groups that were more abundant in the soil cultivated conventionally while it reduced those that were favoured in conservation agriculture.
Potential for and consequences of naturalized Bt products: Qualitative dynamics from indirect intransitivities
2015, Ecological Modelling
Citation Excerpt :
While the authors’ evidence of recurrent introductions of transgenes into landrace genomes was initially debated (Metz and Futterer, 2002; Kaplinsky et al., 2002; see reply, Quist and Chapela, 2002), the primary claim of transgene presence was not. Eventually the presence of GM varieties in Mexico was confirmed by later investigations (Mercer and Wainwright, 2008; Piñeyro-Nelson et al., 2009). Sampling efforts since then have come away with a mix of positive and negative results (Mercer and Wainwright, 2008).
Advances in genetic modification technology and the production of human-altered genomes have led to an array of genetically modified organisms utilized to address numerous global issues. The human need-based development of these modified organisms often presents unprecedented phenotypes which will interact with the world's existing biodiversity in unknown ways. One such example is Bt transgene crops proliferating because of their application to food security issues due to their resistance to pest insects. While threats to long term viability of Bt crop use due to resistance evolution in pests have been extensively investigated, issues regarding the effects of Bt transgene crops on existing ecosystems and the biodiversity contained therein have seen less scrutiny. In particular, the long-term dynamics in the case of a naturalized Bt product has not received the attention it deserves. Here we note that the ecosystem structure emerging from a naturalized Bt crop is, qualitatively, an intransitive loop. Based on this structure we develop a simple ecosystem model showing that the intransitive nature of the system has potential to facilitate long term persistence of naturalized Bt transgenes by shifting community dynamics.
Large scale sampling of Mexican maize landraces for the presence of transgenes
2023, Transgenic Research

View all citing articles on Scopus

¹: Tel.: +1 614 247 8746.

View full text

Gene flow from transgenic maize to landraces in Mexico: An analysis

Abstract

Introduction

Section snippets

Transgene introgression in agricultural systems

Are there transgenes in Mexican maize landraces?

Potential for reduction of transgene frequency in landrace populations

Calls for ‘decontamination’

Potential methods for transgene reduction

Conclusion

Acknowledgements

World Devel.

World Devel.

Biol. Cons.

Peasant agriculture and the conservation of crop and wild plant resources

Conserv. Biol.

Editorial: Negative and positive data, statistical power, and confidence intervals

Environ. Biosaf. Res.

Selected maize statistics

The ethnoecology of maize variety management: a case study from Mexico

Hum. Ecol.

Transgenic maize and the evolution of landrace diversity in Mexico: the importance of farmers’ behavior

Plant Physiol.

Traditional Mexican agricultural systems and the potential impacts of transgenic varieties on maize diversity

Agric. Hum. Val.

Surveying patterns in the cost of resistance in plants

Am. Nat.

Rethinking crop genetic resource conservation

Conserv. Biol.

Maize and Biodiversity: The Effects of Transgenic Maize in Mexico

Los últimos escrutinios de maíz criollo en México no revelan la presencia del promotor relacionado con los transgenes

Detecting (trans)gene flow to landraces in centers of crop origin: lessons from the case of maize in Mexico

Environ. Biosaf. Res.

Population genetic consequences of small population size: implications for plant conservation

Ann. Rev. Ecol. Syst.

Contamination of Bt Genetically Modified Maize in Mexico Much Worse Than Feared

Open Letter from International Civil Society Organizations on Transgenic Contamination in the Centers of Origin and Diversity

Maize Rage in Mexico: GM Maize Contamination in Mexico—2 Years Later

Evidence of gene flow from transgenic maize to local varieties in Mexico

Bioseguridad y actores sociales

Diversity for Development: The Strategy of the International Plant Genetic Resources Institution

Maize transgene results in Mexico are artifacts

Nature