Euphytica (2006) 148: 35–46DOI: 10.1007/s10681-006-5939-3CSpringer 2006Hybridization as a stimulus for the evolution of invasiveness in plants?Norman C. Ellstrand1,∗& Kristina A. Schierenbeck21Department of Botany and Plant Sciences and Center for Conservation Biology, University of California,Riverside, CA 92521-0124, USA;2Department of Biology, California State University, Chico, CA 93740, USA(∗author for correspondence: e-mail: [email protected])Key words: evolution, gene flow, hybrid species, hybridization, invasive plants, weedsSummaryInvasive species are of great interest to evolutionary biologists and ecologists because they represent historicalexamples of dramatic evolutionary and ecological change. Likewise, they are increasingly important economicallyand environmentally as pests. Obtaining generalizations about the tiny fraction of immigrant taxa that becomesuccessful invaders has been frustrated by two enigmatic phenomena. Many of those species that become successfulonly do so (i) after an unusually long lag time after initial arrival, and/or (ii) after multiple introductions. We proposean evolutionary mechanism that may account for these observations. Hybridization between species or betweendisparate source populations may serve as a stimulus for the evolution of invasiveness. We present and review aremarkable number of cases in which hybridization preceded the emergence of successful invasive populations.Progeny with a history of hybridization may enjoy one or more potential genetic benefits relative to their progenitors.The observed lag times and multiple introductions that seem a prerequisite for certain species to evolve invasivenessmay bea correlate of the time necessary for previously isolated populations to come into contact and for hybridizationto occur. Our examples demonstrate that invasiveness can evolve. Our model does not represent the only evolutionarypathway to invasiveness, but is clearly an underappreciated mechanism worthy of more consideration in explainingthe evolution of invasiveness in plants.IntroductionInvasive species have always held a special placefor ecologists and evolutionary biologists. Success-ful invaders that have colonized new regions withinhistorical time provide real-life examples of ecologi-cal and evolutionary change. The demographic changefrom a small number of colonists to a sweeping wave ofinvaders is a dramatic ecological event. Likewise, thosedemographic changes – a founder event followed bya massive increase in numbers – may have dramaticThis paper was presented at the National Academy of Sciencescolloquium “Variation and Evolution in Plants and Microorganisms:Toward a New Synthesis 50 Years After Stebbins,” held January27–29, 2000, at the Arnold and Mabel Beckman Center in Irvine,CA.Reprinted from PNAS 97(13): 7043–7050 (2000).evolutionary consequences. Not surprisingly, wholebooks have been dedicated to the basic science ofinvasive species (for example, see refs. Elton, 1958;Mooney & Drake, 1986).Also, the applied biology of invasive species hasbecome increasingly important as intentional andunintentional anthropogenic dispersal moves speciesfrom continent to continent at unprecedented rates.Invasive plants and animals are often thought of as agri-cultural pests, but they also pose a hazard for a varietyof human concerns, including health, transportation,and conservation (United States Congress, Office ofTechnology Assessment, 1993). Invasive species notonly directly impact human well being, but they alsoare recognized as agents that alter community structureand ecosystem function (for example, see ref. Horvitzet al., 1998). In the United States alone, the damage36wrought by invasive species totals approximately $122billion per year (Pimentel et al., 2000).Only a tiny fraction of introduced species be-come successful invasives (Williamson, 1993). Giventhat invasives are important for so many reasons,considerable effort has been spent trying to developgeneralizations to determine which species are likelyto become successful. In particular, ecological, taxo-nomic, and physiological correlates of invasive suc-cess have been sought to predict which introducedspecies might become successful (for example, seerefs. Bazzaz, 1986; Daehler, 1998; Pyˇsek, 1997; Pyˇsek,1998; Rejmanek, 1996). Less frequently, possible ge-netic correlates have been sought (for example, seeref. Gray, 1986). Very little attention has been givento the possibility of the evolution of invasiveness aftercolonization.Are invasives “born” (that is, are they released fromfitness constraints) or are they “made” (that is, do theyevolve invasiveness after colonization)? The fact thatcertain correlates of invasive success have been iden-tified suggests that invasives are born. Also, Darwin’s(Darwin, 1859) observation that non-native genera aremore likely to be successful invaders than are nativegenera supports the view that successful invasives arepreadapted and do not evolve invasiveness in situ. Cer-tain specific cases of invasives fit this model well. Forexample, the fact that invasiveness can sometimes bereversed by a biological control agent [(e.g., pricklypear in Australia (Dodd, 1959) and Klamath weed inthe American Pacific Northwest (Huffaker & Kennett,1959)] suggests that invasiveness can appear simplyonce an organism is released from its primary biolog-ical enemies. Also, it has been observed that “a strongpredictor of invasiveness ... is whether the organismhas been invasive ...elsewhere” (ref. Ewel et al., 1999p. 627). Although such correlates may be statisticallystrong, they are typically weak in predicting invasions,leading one reviewer of the field to assert, “serendip-ity is often an important element in successful inva-sions” (ref. Gray, 1986, p. 655) and another to lament,“It could be that invasions ... are intrinsically unpre-dictable” (ref. Williamson, 1999, p. 10).But for some successful invasive species, it maywell be that a series of events after colonization is moreimportant than intrinsic “colonizing ability.” In fact,two enigmatic phenomena associated with successfulinvasives suggest that many species are not preadaptedto become successful invasives and that the right cir-cumstances must transpire for invasiveness to occur(and perhaps evolve). The first is the observation thatthere is often a considerable lag phase between the es-tablishment of local populations and their