Abstract
When species hybridize, offspring typically exhibit reduced fitness and maladapted phenotypes. This situation has biosafety implications regarding the unintended spread of novel transgenes, and risk assessments of crop-wild hybrids often assume that poorly adapted hybrid progeny will not evolve adaptive phenotypes. We explored the evolutionary potential of early generation hybrids using nontransgenic wild and cultivated radish (Raphanus raphanistrum, Raphanus sativus) as a model system. We imposed four generations of selection for two weedy traits – early flowering or large size – and measured responses in a common garden in Michigan, USA. Under selection for early flowering, hybrids evolved to flower as early as wild lineages, which changed little. These early-flowering hybrids also recovered wild-type pollen fertility, suggesting a genetic correlation that could accelerate the loss of crop traits when a short life cycle is advantageous. Under selection for large size at reproduction, hybrids evolved longer leaves faster than wild lineages, a potentially advantageous phenotype under longer growing seasons. Although early generation hybrid offspring have reduced fitness, our findings provide novel support for rapid adaptation in crop-wild hybrid populations. Biosafety risk assessment programs should consider the possibility of rapid evolution of weedy traits from early generations of seemingly unfit crop-wild hybrids.
Highlights
When species hybridize, offspring typically exhibit reduced fitness and maladapted phenotypes
Whether the introduced alleles persist in the long-term may be governed by the nature of the introduced trait, the genetic and environmental background in which it is expressed, and levels of local selection, all of which influence the fitness of early generation hybrid offspring (Rissler and Mellon 1996; Arnold 1997; Pialek and Barton 1997; Whitney et al 2006; Wu and Campbell 2006)
Hybrid lineages flowered later than wild lineages (Biotype: F1,3.8 = 25.34, P = 0.009) and both biotypes responded to selection for early flowering (Selection: F1,4.2 = 21.15, P = 0.009)
Summary
When species hybridize, offspring typically exhibit reduced fitness and maladapted phenotypes. The use of experimental hybridization and artificial selection to speed up natural processes allows us to explore ecological scenarios under which the fitness of hybrids lineages may equal or exceed the fitness of their wild parent, favoring the long-term persistence of crop alleles. This combination of evolutionary tools has not been used before in crop-wild hybrids. Populations of crop-wild hybrids may generally experience purifying selection towards the wild phenotype (Hauser et al 1998; Snow and Campbell 2005) and yet occasionally possess neutral or advantageous crop-derived traits, such as resistance to certain diseases or herbicides (e.g., Snow et al 2003; Warren and James 2006; Baack et al 2008; Warwick et al 2008)
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