Population genetics of traditionally managed maize : farming practice as a determinant of genetic structure and identity of maize landraces in Mexico

A large amount of crop genetic diversity is being maintained in farmers' fields worldwide. The population genetics of traditionally managed landraces is therefore of interest to the conservation of genetic resources. The growing trend towards agricultural modernization and the prospect of introducing genetically modified varieties into centers of origin have increased the need to understand the determinants of genetic structure in landraces of our basic food crops. Patterns of genetic diversity are known to be affected by environmental and geographic factors, but there has been an increasing interest in the role of farmers. Recent years have seen work on both genetic differentiation between seedlots, as well as on the agricultural practices that are expected to influence this differentiation. Unfortunately, few studies have been able to link observed patterns of differentiation to farming practice. The lack of a proper analytical framework has probably contributed to this omission. The population genetics of landraces is complex, with many human and environmental factors affecting the distribution of genetic variation. In this thesis, we aim at achieving a better understanding of the processes that underlie the genetic structure maize landraces in their centre of origin, Mexico. We combine a wide range of theoretical and empirical methods in order to provide explanations for observed patterns of genetic structure. In addition, we use these tools to predict some present and future consequences of seed management by farmers on the genetic identity of landrace populations. In chapter II, we present a metapopulation model that accounts for several features that are unique to managed maize populations. We developed a coalescence-based model of a metapopulation undergoing pollen and seed flow as well as extinction in the form of seed replacement. Unlike previous models, our model treats seed migration as episodic-, partial replacement from a single source rather than as constant immigration from the entire metapopulation. We showed that this particular form of migration leads to novel results. Contrary to classical predictions, within-deme coalescence time was not invariant to the amount of migrating seed. Genetic structure had a parabolic relationship to the amount of migrating seed instead of showing the expected exponential decrease. In contrast, the effects of seed migration frequency on diversity and structure were in line with classical predictions. We concluded that is impossible to describe seed migration by a single parameter. Genetic structure was shown to depend on deme size when the amount of migrant seed is large. Extinction decreased or increased genetic structure depending on the level of migration and number of demes. Finally, we demonstrated that higher levels of pollen migration can mask the effects of seed management. This model provides an important first step in our ability to understand the effects of farming practice on the population genetics of maize landraces. In chapter III, we study the joint role of the environment and humans as determinants of genetic differentiation. We present results on the hierarchical genetic structure in a sample of seedlots in highland and lowland environments in central Mexico. Within-and between village Fsl and Qsl values were used as measures of neutral and agronomic genetic differentiation respectively. We developed and used a new computer model to predict Fst in the two environments on the basis of data on local seed management practice and planting patterns. Strong genetic differences were found between highland and lowland maize, for both markers and traits. Three highland villages planted maize of admixed origin, as evidenced by both molecular markers and phenological traits. This suggested that human mediated gene flow from lowland to highland environments has taken place. Molecular differentiation was low for molecular markers but was notably higher in the lowlands. Our model correctly predicted this difference based on lower pollen flow and smaller seedlot sizes in the lowlands. Agronomical traits showed higher differentiation between villages and were probably subject to diversifying selection. Phenological traits showed the strongest differentiation. Field data suggested that different planting dates may explain the observed differences. Phenological differentiation was highest in the transect containing the admixed seedlots, proving that genetic structure may result from the introgression of traits that diverged in a foreign environment. In chapter IV, we address the issue of genetic erosion in modernized subsistence agriculture. Genetic erosion is thought to occur when modern varieties replace traditional landraces. Actual proof of genetic erosion for any particular area or crop has been rarely found however. A complicating factor in the study of diversity loss in traditional agriculture is the often-noted coexistence between traditional and improved varieties. Moreover, adoption of modern varieties into the traditional seed supply system may blur the distinction between modern and traditional varieties. The inability to classify germplasm into discrete types makes it hard to measure diversity. We addressed these problems by means of a case study on modernized smallholder maize agriculture in southern Mexico. We characterized seedlots obtained from both farmers and commercial seed vendors, for agronomical traits and molecular markers. Farmer interviews were used to distinguish between traditional landraces and recycled modern varieties. We calculated genetic diversity, defined as the mean differentiation between individual seedlots, for different types of germplasm. Modem germplasm was clearly distinct from traditional landraces. Close resemblance between modem- and recycled modem varieties proved that despite years of independent evolution, recycled varieties have not diverged much from their ancestral stocks. We showed that different traits reveal different levels of relative diversity, demonstrating the inherent difficulty of assessing diversity loss. The group of recycled modem varieties presented the lowest diversity for all measured traits. We could therefore predict that complete replacement of landraces by these varieties will reduce diversity in the traditional seed system. Under current patterns of coexistence however, the distinctness of modem and traditional varieties caused only a limited reduction of genetic diversity. Chapter V. deals with the effects of reproductive and population genetic processes on the probability of detecting inadvertently introduced transgenes in maize landraces. This subject has become relevant since initial findings suggesting contamination of Mexican landraces with transgenes were followed by contradictory results in subsequent years. Theoretical and simulation results showed that certain aspects of maize reproductive biology negatively affect the detection probability. We demonstrated that the strongest potential limitation on detection was caused by the aggregated frequency distribution that is a consequence of farmer-mediated introduction of transgenes. Analysis of recent sampling efforts reveals that detection probabilities may be much lower than previously assumed, partly explaining the recent inconsistent results 12