Populations of weedy crop–wild hybrid beets show contrasting variation in mating system and population genetic structure

Abstract

Reproductive traits are key parameters for the evolution of invasiveness in weedy crop–wild hybrids. In Beta vulgaris, cultivated beets hybridize with their wild relatives in the seed production areas, giving rise to crop–wild hybrid weed beets. We investigated the genetic structure, the variation in first-year flowering and the variation in mating system among weed beet populations occurring within sugar beet production fields. No spatial genetic structure was found for first-year populations composed of F1 crop–wild hybrid beets. In contrast, populations composed of backcrossed weed beets emerging from the seed bank showed a strong isolation-by-distance pattern. Whereas gametophytic self-incompatibility prevents selfing in wild beet populations, all studied weed beet populations had a mixed-mating system, plausibly because of the introgression of the crop-derived Sf gene that disrupts self-incompatibility. No significant relationship between outcrossing rate and local weed beet density was found, suggesting no trends for a shift in the mating system because of environmental effects. We further reveal that increased invasiveness of weed beets may stem from positive selection on first-year flowering induction depending on the B gene inherited from the wild. Finally, we discuss the practical and applied consequences of our findings for crop-weed management.

Biodiversity Assessment of Sugar Beet Species and Its Wild Relatives: Linking Ecological Data with New Genetic Approaches

“…Also, the different forms of beet clustered into genetic distinctive groups concordant with the classification of cultivated, wild and weedy forms based on their geographical location, phenotype or domesticated status despite the very recent domestication process of sugar beet [42]. High genetic diversity with no isolation-by-distance genetic structure has been commonly found among weed beet populations [41,42,47], although a strong spatial genetic structure was detected in high-density, highly outcrossing populations [48]. This implies that once established, weed beet populations can sustain a high level of genetic variation and thus provide a likely basis for potential rapid evolutionary change.…”

“…Up to now, investigations on the evolutionary dynamics of genetic diversity within the B. vulgaris complex were thus mainly focused on assessing genetic relationships among the different forms of beet [41,42,45,46], with particular emphasis on crop-to-wild gene flow [47,48]. Using a panel of polymorphic markers comprising nuclear microsatellite loci, mitochondrial minisatellite loci and one chloroplastic PCR-RFLP marker, Fénart et al [42] found similar levels of nuclear genetic diversity in weedy beets and sea beets, as opposed to the narrowness of cultivar accessions, but a very strong genetic divergence between wild sea beet and other relatives, which was unexpected given the recent evolutionary history and the full cross-compatibility of all taxa.…”

“…Moreover, characteristics of particular source populations within initial native ranges are likely to shape the evolution of invasive populations [49]. This is particularly true as inland wild beets already adapted to the margins of arable fields and other anthropogenic habitats, through short life-span and first-year flowering, can be found [48]. On the other hand, crop-towild gene flow has been implicated in the increased likelihood of extinction of wild relatives by displacing native wild allelic diversity [47].…”

The red queen in the corn: agricultural weeds as models of rapid adaptive evolution

“…Seed beets are presumed to have been pollinated by wild beets and then planted in sugar beet fields. The weeds persist by undergoing selffertilization (a crop trait), flowering the first year of cultivation (a wild trait), bolting early (a wild trait), and maintaining high levels of seed dormancy (a wild trait), reflecting a mixture of genetic input from wild and cultivated beets (Arnaud et al, 2010). Weedy beet populations do not show evidence of a recent genetic bottleneck, with similar levels of genetic diversity as wild beet populations (Fénart et al, 2008).…”

Eco-Evolutionary Dynamics of Agricultural Networks

“…Here, we will give a brief review of the ways the spatial organization can constrain gene flows, by considering how gene flows have affected the domestication and artificial selection process, how genes flow from cultivated species to surrounding ecosystems, and how agricultural fragmentation affects gene flows among natural populations. Most effort has thus been devoted to measures of contemporaneous gene flow, as measured, for example, in Brassica napus (Hall et al, 2000), Brassica rapa (Warwick et al, 2003;Schafer et al, 2011), Beta vulgaris (Arnaud et al, 2010), and Agrostis stolonifera (Snow, 2012). Gene flows in cultivated-wild/weed complexes have long been recognized as an important process for crop domestication and as a source of crop improvement in traditional agriculture (de Wet and Harlan, 1975;Elias et al, 2001).…”