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Impact of Gene Flow from Cultivated Beet on Genetic Diversity of Wild Sea Beet Populations

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Impact of Gene Flow from Cultivated Beet on Genetic Diversity of Wild Sea Beet Populations MEC769.fm Page 1733 Wednesday, September 29, 1999 9:43 AM Molecular Ecology (1999) 8, 1733–1741 ImpactBlackwell Science, Ltd of gene flow from cultivated beet on genetic diversity of wild sea beet populations DETLEF BARTSCH,* MARC LEHNEN,* JANET CLEGG,† MATTHIAS POHL-ORF,* INGOLF SCHUPHAN* and NORMAN C. ELLSTRAND† *Chair of Biology V, Ecology, Ecochemistry and Ecotoxicology, Aachen University of Technology — RWTH Aachen, D-52056 Aachen, Germany, †Department of Botany and Plant Sciences, University of California, Riverside, CA 92521–0124, USA Abstract Gene flow and introgression from cultivated plants may have important consequences for the conservation of wild plant populations. Cultivated beets (sugar beet, red beet and Swiss chard: Beta vulgaris ssp. vulgaris) are of particular concern because they are cross- compatible with the wild taxon, sea beet (B.vs. ssp. maritima). Cultivated beet seed pro- duction areas are sometimes adjacent to sea beet populations; the numbers of flowering individuals in the former typically outnumber those in the populations of the latter. In such situations, gene flow from cultivated beets has the potential to alter the genetic composition of the nearby wild populations. In this study we measured isozyme allele frequencies of 11 polymorphic loci in 26 accessions of cultivated beet, in 20 sea beet accessions growing near a cultivated beet seed production region in northeastern Italy, and 19 wild beet accessions growing far from seed production areas. We found one allele that is specific to sugar beet, relative to other cultivated types, and a second that has a much higher frequency in Swiss chard and red beet than in sugar beet. Both alleles are typically rare in sea beet populations that are distant from seed production areas, but both are common in those that are near the Italian cultivated beet seed production region, supporting the contention that gene flow from the crop to the wild species can be sub- stantial when both grow in proximity. Interestingly, the introgressed populations have higher genetic diversity than those that are isolated from the crop. The crop-to-wild gene flow rates are unknown, as are the fitness consequences of such alleles in the wild. Thus, we are unable to assess the long-term impact of such introgression. However, it is clear that gene flow from a crop to a wild taxon does not necessarily result in a decrease in the genetic diversity of the native plant. Keywords: Beta vulgaris, gene flow, genetic diversity, introgression, plant conservation genetics, genetically modified plants Received 7 March 1999; revision received 15 June 1998; accepted 15 June 1999 Introduction populations, gene flow may lead to significant evolutionary change in the recipient populations (e.g. Anderson 1949). Domesticated plants often have the potential to spon- Crop-to-weed gene flow will have important practical taneously hybridize with those wild relatives that are and economic consequences if it promotes the evolution growing in close proximity (Ellstrand et al. 1999). Such of more aggressive weeds (e.g. Anderson 1949; Barrett hybridization may lead to gene flow: ‘the incorporation 1983). Hybridization with domesticated species has also of genes into the gene pool of one population from one been implicated in the extinction of certain wild crop or more populations’ (Futuyma 1998). If new or locally relatives (e.g. Small 1984; Ellstrand & Elam 1993). Also, rare alleles from the domesticated plants persist in wild because gene flow tends to genetically homogenize popu- lations (reviewed by Slatkin 1987) and because crops Correspondence: D. Bartsch. Fax: +49 (241) 8888 182; E-mail: are typically genetically depauperate compared to their [email protected] wild relatives (Ladizinsky 1985), overwhelming gene flow © 1999 Blackwell Science Ltd MEC769.fm Page 1734 Wednesday, September 29, 1999 9:43 AM 1734 BARTSCH ET AL. Fig. 1 Geographical distribution of sea beet accessions surveyed in this study (see Table 1). from crops is expected to deplete genetic diversity in wild natural crosses between sugar beet and sea beet in sugar populations (Ellstrand et al. 1999). beet seed production areas, with sea beet as the pollen Over the last decade, much attention has been focused parent. on crop-to-weed hybridization as a potential avenue for The genus Beta is endemic to the Old World. Cultiv- the escape of crop transgenes into natural populations ated beets have been known for more than 2000 years in the (e.g. Colwell et al. 1985; Dale 1994; Darmency 1994). eastern Mediterranean region (Ford-Lloyd & Williams Although that narrow issue has been the topic of numer- 1975). In Europe, wild B.vs. ssp. maritima is largely a coastal ous theoretical, empirical, and synthetic publications, the taxon, with a wide distribution from the Cape Verde general issue of the population genetic consequences of and Canary Islands in the west, northward along Europe’s the flow of alleles from domesticated plants (whether Atlantic coast to the North and Baltic Seas. It extends genetically engineered or not) to their wild relatives has eastward through the Mediterranean region into Asia received scant attention. where it occurs in Asia Minor, in the central and outer Empirical work has been largely focused in two areas: Asiatic steppes and desert areas as far as western India experiments addressing whether a crop and a wild rel- (Letschert 1993). There is no crossing barrier between ative are able to hybridize under field conditions (e.g. wild and cultivated forms of B. vulgaris (Bartsch & Pohl- Langevin et al. 1990; Arias & Rieseberg 1994; Arriola & Orf 1996). Ellstrand 1996; Darmency et al. 1998), and descriptive This study focuses on one of Europe’s most important studies addressing whether introgression from crops has sugar beet seed production districts in northeastern Italy occurred in populations of adjacent wild relatives (e.g. (Fig. 1). Domesticated beet seed production has been in Oka & Chang 1961; Wendel & Percy 1990; Whitton et al. progress in this region for more than 100 years, with 1997; Bartsch & Ellstrand 1999). However, we are not an intensification since the 1950s. All subspecies of B. aware of any study that addresses how population vulgaris are usually wind pollinated, but insect pollination genetic diversity of natural populations is altered under is also possible. In northeastern Italy, commercial sugar gene flow from a crop relative. beet seeds are produced on 4500 ha, each ha containing Therefore, the aim of this study is to examine how gene approximately 50 000 flowering plants. Furthermore, flow and introgression from cultivated beet (Beta vulgaris small farmers in the region grow red beet and Swiss ssp. vulgaris (DC.) HELM) to sea beet (B.vs. ssp. maritima chard for private seed production, which may be an addi- (L.) ARVANG) has impacted upon the genetic diversity tional source of gene flow. Wild sea beet populations of effected wild populations. To date, no population occur on the nearby coastal plain, sometimes within genetic study has been conducted in this gene flow 1000 m of the cultivated fields. All red beet and Swiss direction in Beta, but there are several reports of gene chard cultivars are diploid, as is the wild sea beet. The flow from wild to cultivar populations. Weed beets have most common varieties of sugar beet are diploid. How- appeared in sugar beet fields in France (Boudry et al. ever, some tetraploid sugar beet cultivar lines are used to 1993; Desplanque et al. 1999) and the UK (Hornsey & breed triploid varieties by crosses with diploids (Barocka Arnold 1979; Ford-Lloyd & Hawkes 1986) as a result of 1985). Previous studies demonstrated that genetically © 1999 Blackwell Science Ltd, Molecular Ecology, 8, 1733–1741 MEC769.fm Page 1735 Wednesday, September 29, 1999 9:43 AM GENE FLOW FROM CULTIVATED BEET TO SEA BEET 1735 Table 1a Cultivated Beta vulgaris accessions surveyed in this study No. Taxon Variety/Type Accession Origin Ploidy N 01 B. vulgaris ssp. vulgaris sugar beet USDA FC172 USA 2 15 02 KWS-2N1009 Germany 2 30 03 KWS-Kavetina Germany 3 49 04 KWS-Rizor Germany 2 48 05 KWS-246 Italy 2 39 06 KWS-247 Italy 3 41 07 Betaseed-4035 USA 2 25 08 Betaseed-4581 USA 2 24 09 Betaseed-4776 USA 2 31 10 SES-HH103 USA 2 29 11 Spreckels-IV2R USA 2 30 12 Spreckels-NB2 USA 2 34 13 Spreckels-SS781 USA 2 85 14 Spreckels-VB7R USA 2 26 15 B. vulgaris ssp. vulgaris Swiss chard Dark Green USA 2 70 16 Fordhook USA 2 21 17 Lucullus Germany 2 21 18 Rhubarb USA 2 39 19 Glatter Silber Germany 2 20 20 B. vulgaris ssp. vulgaris Red beet USDA W300C USA 2 32 21 Burpee USA 2 78 22 Detroit Dark Red USA 2 16 23 Red Ball USA 2 25 24 Tall Top USA 2 29 25 Forono Germany 2 20 26 Rubia Germany 2 20 N, number of individuals examined. based morphological markers that are crop specific occa- Materials and methods sionally occur in the wild populations, revealing that some gene flow occurs in this region from 2.25 × 108 flower- Plant materials ing sugar beets into populations of approximately 4 × 104 flowering wild beets over an area of 4000 km2 (Bartsch & We assayed allozyme diversity in 69 wild and cultivated Schmidt 1997; Bartsch & Brand 1998). Beta accessions. We obtained samples from seed com- We used allozymes to characterize the genetic vari- panies (mostly diploid, but also one triploid, sugar beet ation within accessions of cultivated beet (sugar beet, material), from international plant genetic resource collec- Swiss chard, and red beet), accessions of wild sea beet tions or from collecting directly from wild populations adjacent to the cultivated beet seed production region of (Table 1a,b). Accessions were selected to represent a wide northeastern Italy, and accessions of wild sea beet from geographical range of wild beets (Fig.
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