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Pollinator Preferences and the Persistence of Crop Genes in Wild Radish Populations (Raphanus Raphanistrum, Brassicaceae)1

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Pollinator Preferences and the Persistence of Crop Genes in Wild Radish Populations (Raphanus Raphanistrum, Brassicaceae)1 American Journal of Botany 85(3): 333±339. 1998. POLLINATOR PREFERENCES AND THE PERSISTENCE OF CROP GENES IN WILD RADISH POPULATIONS (RAPHANUS RAPHANISTRUM, BRASSICACEAE)1 TED N. LEE2, 4 AND ALLISON A. SNOW3, 5 2Department of Biology, University of Michigan, 830 N. University, Ann Arbor, Michigan 48109±1048; and 3Department of Plant Biology, Ohio State University, 1735 Neil Avenue, Columbus, Ohio 43214 Crop±weed hybridization can potentially in¯uence the evolutionary ecology of wild populations. Many crops are known to hybridize with wild relatives, but few studies have looked at the long-term persistence of crop genes in the wild. This study investigated one factor in the hybridization process in radish: differential pollinator visitation to wild radish (Raphanus raphanistrum) vs. crop±wild F1 hybrids (R. sativus 3 R. raphanistrum). Wild genotypes had yellow ¯owers, a recessive single-locus trait, whereas hybrids always had white or pale pink ¯owers. In experimental arrays in northern Michigan, total pollinator visitation was signi®cantly biased toward wild plants when the frequencies of wild and hybrid plants were equal. Syrphid ¯ies, the most frequent visitors, preferred wild plants while bumble bees showed no preference. This pattern was also observed when hybrid plants were overrepresented in the array (12 hybrid : 2 wild). In contrast, when hybrid plants were rare (2 hybrid : 12 wild), neither morph was preferred by any pollinator group. Later in the summer, pollinators were also observed in a large experimental garden with nearly equal frequencies of wild and hybrid plants. Cabbage butter¯ies (Pieris rapae) strongly overvisited wild plants, while bumble bees showed a slight preference for hybrids. Taken together, these studies suggest that F1 hybrids may not be at a disadvantage with regard to pollinator visits when they occur at low frequencies or when bumble bees are frequent ¯ower visitors. Thus, variation in the proportion of white-¯owered morphs among wild radish populations could be in¯uenced by different histories of crop-to-wild hybridization, as well as by variation in the composition of local pollinator taxa. Key words: Brassicaceae; bumble bee; butter¯y; ¯ower color; hybridization; pollination; radish; Raphanus; syrphid. Spontaneous hybridization between crops and their 1994). In this study, we focus on another wild radish wild relatives may promote rapid evolution in weeds species, Raphanus raphanistrum, which is capable of hy- (e.g., Small, 1984). Recently, the greatest ecological con- bridizing with wild and cultivated R. sativus (Panetsos cern regarding crop±weed hybridization has been that and Baker, 1967). bene®cial engineered genes (transgenes) inserted into Wild radish (Raphanus raphanistrum) is an agricultur- crop plants will escape into wild populations via pollen al weed from Eurasia that occurs on several continents, dispersal, thus potentially increasing the invasiveness of including northeastern North America (Holm et al., natural relatives (see reviews in Raybould and Gray, 1979). As a self-incompatible annual, it is an obligate 1993; Snow and MoraÂn Palma, 1997). Crop±weed hy- outcrosser that relies on insect pollinators for successful bridization occurs frequently in a wide range of poten- reproduction (e.g., Stanton et al., 1989; Conner and Rush, tially weedy plants, including canola (Brassica rapa, Ad- 1996; Kercher and Conner, 1996). R. raphanistrum is ler et al., 1993; B. napus 3 B. campestris, Jùrgensen and polymorphic for ¯ower color (yellow or white), and al- Andersen, 1995), sorghum and johnsongrass (Sorghum though the white allele is dominant to yellow in a single- bicolor 3 S. halapense, Arriola and Ellstrand, 1996), sun- locus system (Kay, 1978; Stanton et al., 1989), white- ¯ower (Helianthus annuus, Arias and Rieseberg, 1994), ¯owered plants are often rare or absent in wild popula- squash (Cucurbita texana 3 C. pepo, Kirkpatrick and tions (Kercher and Conner, 1996; A. Snow, unpublished Wilson, 1988), and wild radish (Raphanus sativus, Klin- data). The presence of these white morphs may be a result ger, Elam, and Ellstrand, 1991; Klinger and Ellstrand, of hybridization with cultivated radish (R. sativus, Kay, 1984; Kercher and Conner, 1996). If this is the case, dif- 1 Manuscript received 2 December 1996; revision accepted 15 July ferent histories of hybridization between wild and culti- 1997. vated radish could alter ¯ower color frequencies in wild The authors thank Sara Beresford, Dave Karowe, and Joe Holomuski populations. The goal of this study was to determine for their invaluable contributions to this study; Jeffrey Karron and an whether differential pollinator visitation to these ¯ower anonymous reviewer for comments on the manuscript; Jeff Conner for color morphs could also in¯uence the spread and persis- seeds from Bay City, Michigan; Dave Cowan for assistance with insect identi®cation; and Bob VandeKopple and the University of Michigan tence of crop genes, especially the white allele and others Biological Station staff for valuable logistical assistance. This study was that are linked to this locus. supported by a grant from NSF's Research Experience for Undergrad- Pollinators often discriminate between petal color var- uates program, the Biddeford Fund (OSU), and the University of Mich- iants of polymorphic species (Phlox drummondii, Levin, igan Biological Station. 1972a, b; Levin and Brack, 1995; Delphinium nelsonii, 4 Author for correspondence, current address: Department of Ecology Waser and Price, 1981, 1983; Ipomoea purpurea, Brown and Evolutionary Biology, University of Arizona, Tucson, AZ 85721- 0066 (e-mail: [email protected]). and Clegg, 1984; Schoen and Clegg, 1985; Epperson and 5 Also at the University of Michigan Biological Station, Pellston, MI, Clegg, 1987; R. sativus, Stanton, 1987; R. raphanistrum, 49769. Stanton, Snow, and Handel, 1986; Stanton et al., 1989). 333 334 AMERICAN JOURNAL OF BOTANY [Vol. 85 Such behavior may in¯uence the relative reproductive success of color morphs by biasing maternal and paternal contributions to the next generation towards the more fre- quently visited morph. For example, Pieris rapae (cab- bage butter¯y) strongly preferred the yellow-¯owered morph of wild radish over the white (Kay, 1976) and this preference affected the relative paternal success of the two morphs (Stanton, Snow, and Handel, 1986; Stanton et al., 1989). The present study is unique in that (1) we test for effects of ¯ower color frequencies on pollinator behavior, (2) we provide data on additional types of pol- linators of wild radish, and (3) we focus on how polli- Fig. 1. Array for experimental radish populations (7y : 7w) where nator preferences in¯uence the introgression of genes underlined numbers signify white-¯owered plants and plain numbers from cultivated radish (R. sativus) into wild populations are yellow. of R. raphanistrum. The dynamics of pollen movement between these two species has not been studied previ- ously, despite the fact that R. sativus is commonly grown arranged in an array of four interconnecting hexagons (Fig. 1). All on farms and in home gardens across the United States plants were comparable in size and ¯ower number and were spaced and hybridization between them is probable (Panetsos 0.75 m from adjacent plants. We did not attempt to arti®cially maintain and Baker, 1967; Kercher and Conner, 1996). equal numbers of ¯owers on each plant because the plants were also In this study, we compared visitation rates to crop±wild being monitored for ¯ower production and fruit set (A. Snow, unpub- F1 hybrids (R. sativus 3 R. raphanistrum, white or pale lished data). The positions of white and yellow plants were rotated pink ¯owers) vs. purely wild plants (R. raphanistrum, among trials to prevent possible edge effects. yellow ¯owers) to address the following questions: (1) To assess whether pollinator preferences were frequency dependent, Do pollinators prefer one petal color variant over an- two additional array designs were used. Rather than containing equal other? (2) Are preferences consistent among pollinator numbers of white and yellow plants, each array was composed of either taxa? (3) Are pollinator preferences in¯uenced by the rel- 12 white and two yellow plants (12w : 2y, yellows rare), or two white ative frequencies of wild and hybrid plants in a popula- and 12 yellow plants (2w : 12y, whites rare). In these designs, rare plants tion? were placed at positions 7 and 9 in the hexagonal array (Fig. 1). Four replicates of each of the three array designs were conducted in random MATERIALS AND METHODS order over a 12-d period, and we observed one array design per day for ;4.5 h. Source of plants and inheritance of ¯ower colorÐSeeds of R. ra- phanistrum were collected in Bay City, Michigan (same population as Pollinator observationsÐFor each ¯ower visitor, we recorded the described in Kercher and Conner, 1996). Yellow-¯owered plants grown taxon (bumble bee, syrphid ¯y, or other), ¯ower color of the plant from these seeds were hand-pollinated with pollen from each other or visited, number of ¯owers visited per plant, and the position of the plant from cultivated radish plants (Scarlet Globe: a commonly grown culti- within the array. Visits were recorded only when the insect probed the var in this region) to obtain wild and hybrid F1 progeny for the exper- ¯ower for nectar and/or pollen. Preferences were determined by com- iments described below. Flowers of Scarlet Globe radishes were white, paring the number of visits to each color morph with expected values pale pink, or pink. All wild 3 wild progeny had yellow ¯owers as based on ¯ower color frequencies in each array (chi-square tests). Ex- expected, while most of the interspeci®c hybrids were white-¯owered. pected values for plant-to-plant visits were calculated from ratios of Although a few hybrid plants had pale pink ¯owers, for brevity the white- and yellow-¯owered plants, while those for individual ¯ower hybrids will be referred to as white-¯owered below. visits were calculated from the numbers of white and yellow ¯owers Preliminary studies showed that the locus determining white or yel- on all plants in the array for each day.
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