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Raphanus Sativus) Biol Invasions (2009) 11:2251–2264 DOI 10.1007/s10530-008-9412-1 ORIGINAL PAPER Evolution of enhanced reproduction in the hybrid-derived invasive, California wild radish (Raphanus sativus) Caroline E. Ridley Æ Norman C. Ellstrand Received: 18 November 2007 / Accepted: 5 December 2008 / Published online: 25 December 2008 Ó The Author(s) 2008. This article is published with open access at Springerlink.com Abstract Evolution is receiving increased attention genotype-by-environment interaction, indicating that as a potentially important factor in invasions. For maintenance of genetic and phenotypic diversity example, hybridization may have stimulated the between populations may be responsible for the evolution of invasiveness in several well-known weed’s ability to invade a wide breadth of California plant pests. However, the mechanism for success of habitats. Our results suggest that hybridization may such hybrid-derived lineages remains unknown in the contribute the evolution of enhanced invasiveness majority of the cases studied. Here we ask whether and, also, that by limiting the introduction and increased reproductive success (in terms of maternal subsequent hybridization of congeners, we may be fitness) has evolved in an invasive lineage with able to prevent the evolution of new invasive confirmed hybrid ancestry. We compare the relative lineages. fitness of the non-native, hybrid-derived California wild radish (Raphanus sativus) to that of its two Keywords Common garden experiment Á progenitor species in field experiments at different Fitness traits Á Genotype 9 environment interaction Á sites and in different years. We found that California Hybridization Á Invasiveness Á Raphanus wild radish has high survivorship and produces more fruits per plant and more seeds per plant than either of its progenitors in several environments. Furthermore, Introduction populations of California wild radish display a strong Evidence is mounting that evolution can be an important factor in the invasion process (Barrett et al. 2008; Cox 2004; Dlugosch and Parker 2008; C. E. Ridley Á N. C. Ellstrand Keller and Taylor 2008; Lambrinos 2004; Lee 2002). Department of Botany and Plant Sciences, University Evolutionary change can be rapid and substantial in of California, Riverside, CA 92521, USA introduced populations, in some cases stimulating the creation of novel, highly invasive genotypes (Dlu- N. C. Ellstrand Center for Conservation Biology, University gosch and Parker 2008; Ellstrand and Schierenbeck of California, Riverside, CA 92521, USA 2006). Hybridization, defined as the successful mating of & C. E. Ridley ( ) two genetically distinct sources (e.g., Arnold 1997), Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108, USA could be quite common in populations of non-native, e-mail: [email protected] sexually reproducing species because introductions 123 2252 C. E. Ridley, N. C. Ellstrand often originate from multiple and/or geographically charlock, arrived accidentally, probably as a weed diverse source populations (e.g., Bartlett et al. 2002; contaminant of grain (Panetsos and Baker 1967; Durka et al. 2005; Genton et al. 2005; Maron et al. Robbins 1940). Native to the Mediterranean, R. 2004; Marrs et al. 2008; Novak and Mack 2001). raphanistrum has been listed as one of the world’s Such intraspecific hybridization has been implicated worst weeds (Holm et al. 1997) and is an agricultural in enhancing invasiveness in several species, includ- pest in Canada, the northern United States and ing both plants and animals (Facon et al. 2005; Australia (Snow and Campbell 2005). Both R. sativus Lavergne and Molofsky 2007). Many well-known and R. raphanistrum are annual and self-incompati- examples of interspecific hybrid invaders also exist. ble. The two species are differentiated by a number of Spartina anglica in Britain is derived from the genetically-based traits including root morphology, hybridization of an introduced species, S. alterniflora, fruit morphology, flower color and flowering time with the native S. maritima, while the hybrid lineage (Hegde et al. 2006; Panetsos and Baker 1967). They between introduced S. alterniflora and the native S. also differ from one another by a single chromosomal foliosa is invading the West Coast of North America reciprocal translocation that results in partial repro- (Ainouche et al. 2004; Ayres et al. 2003). ductive isolation via 50% reduced fertility in the F1 Although several coincidences of hybridization generation (Panetsos and Baker 1967). This repro- with invasion have been identified (Ellstrand and ductive barrier is easily overcome, however, such that Schierenbeck 2006), the mechanisms by which later generation hybrids have substantially recovered hybrid-derived lineages establish and spread have fertility (Snow and Campbell 2005). been rarely studied. The simplest explanation might As late as the 1960s, both morphologically pure be that hybridization creates genotypes that are more populations of each introduced Raphanus species and reproductively successful than the pure progenitor clearly hybrid-derived populations were not uncom- genotypes, perhaps as a result of fixed heterosis, the mon in coastal and inland northern California purging of deleterious alleles or the transfer of (Panetsos and Baker 1967). Some 40 years later, in adaptations (Ellstrand and Schierenbeck 2006; Riese- a wide sampling of Raphanus throughout the state, berg et al. 1999). All other things being equal, a hybrid genetic ancestry was found for every popula- lineage that reproduces more is likely to be more tion (Hegde et al. 2006; Ridley et al. 2008). Thus, invasive because of the prime importance of propa- over the last century, the two Raphanus species have gule pressure during the invasion process (Colautti coalesced into a hybrid lineage that has displaced all et al. 2006; Hayes and Barry 2008; Lockwood et al. natural populations of both parents. Commonly 2005). Increased genetic diversity relative to progen- referred to as ‘‘California wild radish’’, this lineage itor populations might also affect the success of is now found throughout a major portion of naturally hybrid-derived populations by enhancing their ability disturbed coastal areas and human-disturbed inland to respond to selection and to adaptively evolve sites in California (DiTomaso and Healy 2006; (Ellstrand and Schierenbeck 2006; Lee 2002; Parker Panetsos and Baker 1967), as well as south into Baja et al. 2003; Sakai et al. 2001). However, hybrid- California, Mexico and north into Oregon (Hegde derived lineages do not necessarily have to display a et al. 2006; Ridley 2008). Interestingly, interspecific reproductive advantage to be more invasive than their Raphanus hybrids also appear in Europe, but are not introduced progenitors (Bergelson 1994). In theory, invasive (Stace 1975). they could show one of the other qualities of a good Raphanus is an important model system. Plant invader, such as superior competitive or dispersal ecologists, evolutionists and geneticists have all used ability. Our system, the California wild radish Raphanus for studying pollination biology, life- (Raphanus sativus), is an extensively studied non- history variation, ecological genetics, floral evolution native lineage that is appropriate for examining the and plant-herbivore interactions (e.g., Campbell et al. mechanism (s) of hybrid invasive success. 2006; Conner 1997; Elam et al. 2007; Ellstrand et al. In the mid-1800s, two Raphanus species colonized 1989; Irwin et al. 2003; Marshall and Diggle 2001; the San Francisco Bay area of California. Cultivated Mazer and Schick 1991; Stanton et al. 1991). radish R. sativus was introduced intentionally as a Here, we use a common garden field experiment crop. Raphanus raphanistrum, also known as jointed to gain evidence for one mechanism by which 123 Evolution of enhanced reproduction in the hybrid-derived invasive 2253 California wild radish has replaced its progenitors on of R. raphanistrum were likewise chosen to represent the western coast of North America. Phenotypically, the species’ geographic range, including sites from California wild radish tends to show intermediacy to which plants could have been introduced to Califor- its progenitor species for many traits, including nia. Seeds from native habitat in Europe (Denmark) bolting and flowering dates, and root length and and two naturalized populations from North America width, but it exceeds both progenitors for average (Mexico and Rhode Island) were included. The R. fruit weight, a potential fitness correlate (Hegde et al. raphanistrum populations chosen had no evidence of 2006). In addition, advanced generation artificial R. prior introgression from the crop. Cultivars are likely sativus 9 R. raphanistrum hybrids grown in southern ancestors of the current CA wild radish populations California have shown a significant survival and based on molecular analysis (Ellstrand and Marshall reproductive advantage over the weedy progenitor, R. 1985; Ridley et al. 2008). raphanistrum (Campbell et al. 2006). Given this To obtain sufficient seed for multiple years of field evidence, we hypothesize that the naturally hybrid- studies, seed was multiplied from the original CA derived California wild radish will show enhanced wild radish and R. raphanistrum populations two fitness relative to the species that hybridized to create times: once in 2004 for a 2005 common garden and it, and that this could be one mechanism for its again in 2005 for two common gardens planted
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