Selection on Crop-Derived Traits and QTL in Sunflower (Helianthus annuus) Crop-Wild Hybrids under Water Stress Birkin R. Owart 1 , Jonathan Corbi 2 , John M. Burke 2 , Jennifer M. Dechaine 1 * 1 Department of Biological Sciences, Central Washington University, Ellensburg, Washington, United States of America, 2 Department of Plant Biology, University of Georgia, Athens, Georgia, United States of America Abstract Locally relevant conditions, such as water stress in irrigated agricultural regions, should be considered when assessing the risk of crop allele introgression into wild populations following hybridization. Although research in cultivars has suggested that domestication traits may reduce fecundity under water stress as compared to wild-like phenotypes, this has not been investigated in crop-wild hybrids. In this study, we examine phenotypic selection acting on, as well as the genetic architecture of vegetative, reproductive, and physiological characteristics in an experimental population of sunflower crop- wild hybrids grown under wild-like low water conditions. Crop-derived petiole length and head diameter were favored in low and control water environments. The direction of selection differed between environments for leaf size and leaf pressure potential. Interestingly, the additive effect of the crop-derived allele was in the direction favored by selection for approximately half the QTL detected in the low water environment. Selection favoring crop-derived traits and alleles in the low water environment suggests that a subset of these alleles would be likely to spread into wild populations under water stress. Furthermore, differences in selection between environments support the view that risk assessments should be conducted under multiple locally relevant conditions. Citation: Owart BR, Corbi J, Burke JM, Dechaine JM (2014) Selection on Crop-Derived Traits and QTL in Sunflower (Helianthus annuus) Crop-Wild Hybrids under Water Stress. PLoS ONE 9(7): e102717. doi:10.1371/journal.pone.0102717 Editor: William J. Etges, University of Arkansas, United States of America Received March 3, 2014; Accepted June 21, 2014; Published July 21, 2014 Copyright: ß 2014 Owart et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the United States Department of Agriculture Biotechnology Risk Assessment Program competitive grant #2010-33522- 21668 from the United States Department of Agriculture – National Institute of Food and Agriculture. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * Email: dechaine@cwu.edu Introduction Although gene flow from cultivated to wild populations has likely been occurring since the domestication of wild lineages, interest in the topic has increased with the commercialization of transgenic crops. Consequences of crop-wild hybridization may include the escape of engineered genes into wild populations [1], increased invasiveness of wild relatives of the cultivar [2] [3], and the potential for crop-wild hybrids to outcompete native taxa [4]. Crop-wild hybridization must thus be considered when discussing the potential impacts of transgenic cultivars. The selective advantage of an allele is the best predictor of its establishment and spread in a new population [5] [6], and potentially advantageous transgenic alleles have been documented in Cucurbita pepo [7], Helianthus annuus [8], and Oyrza sativa [9]. These studies suggest that transgenes can increase fitness in crop-wild individuals following introgression, but the ubiquity of their effects on wild populations under diverse selective environ- ments is largely unknown. Although much attention has been given to the escape of engineered transgenes, crop-wild hybridization may also contrib- ute advantageous natural alleles to wild populations and can thus be used to model how selection acts on potential targets for genetic engineering. Hybridization between non-transgenic cultivars and wild relatives has resulted in the generation of at least seven types of agricultural weeds [10], and range expansion of wild populations following crop-derived allele introgression has been observed in Sorghum halapense, Rhododendron ponticum, and Manihot reptans [11]. Studies in sunflower have suggested that crop-like traits (i.e., earlier flowering time and a larger primary inflorescence) increase reproductive output in crop-wild hybrids under a range of natural conditions [12] [13]. Crop-derived alleles have been known to persist within wild populations for at least five generations following hybridization in sunflower [14] and ten generations in wild radish [15], suggesting that some crop-derived alleles may persist in the wild, contrary to expectation. Indeed, crop-derived alleles may have also contributed to the evolution of weediness in wild sunflower [16]. Estimations of selection for crop- derived traits and alleles in wild environments may be applied toward understanding the consequences of transgene escape into the wild. The fitness effects of a trait or allele likely differ with environmental factors. For example, when exposed to increased interspecific competition and herbicide application, the relative fitness of sunflower crop-wild hybrids increased compared to their wild counterparts, suggesting that crop-like traits are more advantageous under certain conditions [17] [18]. Studies in sunflower also show that crop-like flowering (early) was advanta- geous in the absence of herbivory [12] [13], but wild-like flowering (later) was favored when pre-dispersal herbivory was considered PLOS ONE | www.plosone.org 1 July 2014 | Volume 9 | Issue 7 | e102717