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Fitness of crop-wild hybrid sunflower under competitive conditions: implications for crop-to-wild introgression.

ABSTRACT: Understanding the likelihood and extent of introgression of novel alleles in hybrid zones requires comparison of lifetime fitness of parents and hybrid progeny. However, fitness differences among cross types can vary depending on biotic conditions, thereby influencing introgression patterns. Based on past work, we predicted that increased competition would enhance introgression between cultivated and wild sunflower (Helianthus annuus) by reducing fitness advantages of wild plants. To test this prediction, we established a factorial field experiment in Kansas, USA where we monitored the fitness of four cross types (Wild, F1, F2, and BCw hybrids) under different levels of interspecific and intraspecific competition. Intraspecific manipulations consisted both of density of competitors and of frequency of crop-wild hybrids. We recorded emergence of overwintered seeds, survival to reproduction, and numbers of seeds produced per reproductive plant. We also calculated two compound fitness measures: seeds produced per emerged seedling and seeds produced per planted seed. Cross type and intraspecific competition affected emergence and survival to reproduction, respectively. Further, cross type interacted with competitive treatments to influence all other fitness traits. More intense competition treatments, especially related to density of intraspecific competitors, repeatedly reduced the fitness advantage of wild plants when considering seeds produced per reproductive plant and per emerged seedling, and F2 plants often became indistinguishable from the wilds. Wild fitness remained superior when seedling emergence was also considered as part of fitness, but the fitness of F2 hybrids relative to wild plants more than quadrupled with the addition of interspecific competitors and high densities of intraspecific competitors. Meanwhile, contrary to prediction, lower hybrid frequency reduced wild fitness advantage. These results emphasize the importance of taking a full life cycle perspective. Additionally, due to effects of exogenous selection, a given hybrid generation may be especially well-suited to hastening introgression under particular environmental conditions.

SUBMITTER: Mercer KL

PROVIDER: S-EPMC4189920 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: After crop-wild hybridization, some of the crop genomic segments may become established in wild populations through selfing of the hybrids or through backcrosses to the wild parent. This constitutes a possible route through which crop (trans)genes could become established in natural populations. The likelihood of introgression of transgenes will not only be determined by fitness effects from the transgene itself but also by the crop genes linked to it. Although lettuce is generally regarded as self-pollinating, outbreeding does occur at a low frequency. Backcrossing to wild lettuce is a likely pathway to introgression along with selfing, due to the high frequency of wild individuals relative to the rarely occurring crop-wild hybrids. To test the effect of backcrossing on the vigour of inter-specific hybrids, Lactuca serriola, the closest wild relative of cultivated lettuce, was crossed with L. sativa and the F(1) hybrid was backcrossed to L. serriola to generate BC(1) and BC(2) populations. Experiments were conducted on progeny from selfed plants of the backcrossing families (BC(1)S(1) and BC(2)S(1)). Plant vigour of these two backcrossing populations was determined in the greenhouse under non-stress and abiotic stress conditions (salinity, drought, and nutrient deficiency). RESULTS: Despite the decreasing contribution of crop genomic blocks in the backcross populations, the BC(1)S(1) and BC(2)S(1) hybrids were characterized by a substantial genetic variation under both non-stress and stress conditions. Hybrids were identified that performed equally or better than the wild genotypes, indicating that two backcrossing events did not eliminate the effect of the crop genomic segments that contributed to the vigour of the BC(1) and BC(2) hybrids. QTLs for plant vigour under non-stress and the various stress conditions were detected in the two populations with positive as well as negative effects from the crop. CONCLUSION: As it was shown that the crop contributed QTLs with either a positive or a negative effect on plant vigour, we hypothesize that genomic regions exist where transgenes could preferentially be located in order to mitigate their persistence in natural populations through genetic hitchhiking.

Project description:Abiotic and biotic heterogeneity result in divergent patterns of natural selection in nature, with important consequences for fundamental evolutionary processes including local adaptation, speciation, and diversification. However, increasing amounts of the global terrestrial surface are homogenized by agriculture (which covers nearly 50% of terrestrial vegetated land surface) and other anthropogenic activities. Agricultural intensification leads to highly simplified biotic communities for many taxa, which may alter natural selection through biotic selective agents. In particular, the presence of crops may alter selection on traits of closely related wild relatives via shared mutualists and antagonists such as pollinators and herbivores. We asked how the presence of crop sunflowers (Helianthus annuus) alters natural selection on reproductive traits of wild sunflowers (Helianthus annuus texanus). Across two years and multiple sites, we planted replicated paired populations of wild H. a. texanus bordering sunflower crop fields versus approximately 2.5 km away. We measured fitness, floral traits, and interactions of the plants with insect pollinators and seed predators. We found limited evidence that proximity to crop sunflowers altered selection on individual traits, as total or direct selection differed by proximity for only three of eleven traits: ray length (a marginally significant effect), Isophrictis (Gelechiidae, moth) attack, and Neolasioptera (Cecidomyiidae, midge) attack. Direct (but not total) selection was significantly more heterogenous far from crop sunflowers relative to near crop sunflowers. Both mutualist pollinators and antagonist seed predators mediated differences in selection in some population-pairs near versus far from crop sunflowers. Here, we demonstrate that agriculture can influence the evolution of wild species via altered selection arising from shared biotic interactions, complementing previously demonstrated evolutionary effects via hybridization.

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Fitness of crop-wild hybrid sunflower under competitive conditions: implications for crop-to-wild introgression.

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