Evolution of enhanced reproduction in the hybridd

Authors: Caroline E Ridley Norman C Ellstrand

Publish Date: 2008/12/25

Volume: 11, Issue: 10, Pages: 2251-

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Abstract

Evolution is receiving increased attention as a potentially important factor in invasions For example hybridization may have stimulated the evolution of invasiveness in several wellknown plant pests However the mechanism for success of such hybridderived lineages remains unknown in the majority of the cases studied Here we ask whether increased reproductive success in terms of maternal fitness has evolved in an invasive lineage with confirmed hybrid ancestry We compare the relative fitness of the nonnative hybridderived California wild radish Raphanus sativus to that of its two progenitor species in field experiments at different sites and in different years We found that California 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 populations of California wild radish display a strong genotypebyenvironment interaction indicating that maintenance of genetic and phenotypic diversity between populations may be responsible for the weed’s ability to invade a wide breadth of California habitats Our results suggest that hybridization may contribute the evolution of enhanced invasiveness and also that by limiting the introduction and subsequent hybridization of congeners we may be able to prevent the evolution of new invasive lineagesEvidence is mounting that evolution can be an important factor in the invasion process Barrett et al 2008 Cox 2004 Dlugosch and Parker 2008 Keller and Taylor 2008 Lambrinos 2004 Lee 2002 Evolutionary change can be rapid and substantial in introduced populations in some cases stimulating the creation of novel highly invasive genotypes Dlugosch and Parker 2008 Ellstrand and Schierenbeck 2006Hybridization defined as the successful mating of two genetically distinct sources eg Arnold 1997 could be quite common in populations of nonnative sexually reproducing species because introductions often originate from multiple and/or geographically diverse source populations eg Bartlett et al 2002 Durka et al 2005 Genton et al 2005 Maron et al 2004 Marrs et al 2008 Novak and Mack 2001 Such intraspecific hybridization has been implicated in enhancing invasiveness in several species including both plants and animals Facon et al 2005 Lavergne and Molofsky 2007 Many wellknown examples of interspecific hybrid invaders also exist Spartina anglica in Britain is derived from the hybridization of an introduced species S alterniflora with the native S maritima while the hybrid lineage between introduced S alterniflora and the native S foliosa is invading the West Coast of North America Ainouche et al 2004 Ayres et al 2003Although several coincidences of hybridization with invasion have been identified Ellstrand and Schierenbeck 2006 the mechanisms by which hybridderived lineages establish and spread have been rarely studied The simplest explanation might be that hybridization creates genotypes that are more reproductively successful than the pure progenitor genotypes perhaps as a result of fixed heterosis the purging of deleterious alleles or the transfer of adaptations Ellstrand and Schierenbeck 2006 Rieseberg et al 1999 All other things being equal a lineage that reproduces more is likely to be more invasive because of the prime importance of propagule pressure during the invasion process Colautti et al 2006 Hayes and Barry 2008 Lockwood et al 2005 Increased genetic diversity relative to progenitor populations might also affect the success of hybridderived populations by enhancing their ability to respond to selection and to adaptively evolve Ellstrand and Schierenbeck 2006 Lee 2002 Parker et al 2003 Sakai et al 2001 However hybridderived lineages do not necessarily have to display a reproductive advantage to be more invasive than their introduced progenitors Bergelson 1994 In theory they could show one of the other qualities of a good invader such as superior competitive or dispersal ability Our system the California wild radish Raphanus sativus is an extensively studied nonnative lineage that is appropriate for examining the mechanism s of hybrid invasive successIn the mid1800s two Raphanus species colonized the San Francisco Bay area of California Cultivated radish R sativus was introduced intentionally as a crop Raphanus raphanistrum also known as jointed charlock arrived accidentally probably as a weed contaminant of grain Panetsos and Baker 1967 Robbins 1940 Native to the Mediterranean R raphanistrum has been listed as one of the world’s worst weeds Holm et al 1997 and is an agricultural pest in Canada the northern United States and Australia Snow and Campbell 2005 Both R sativus and R raphanistrum are annual and selfincompatible The two species are differentiated by a number of geneticallybased traits including root morphology fruit morphology flower color and flowering time Hegde et al 2006 Panetsos and Baker 1967 They also differ from one another by a single chromosomal reciprocal translocation that results in partial reproductive isolation via 50 reduced fertility in the F 1 generation Panetsos and Baker 1967 This reproductive barrier is easily overcome however such that later generation hybrids have substantially recovered fertility Snow and Campbell 2005As late as the 1960s both morphologically pure populations of each introduced Raphanus species and clearly hybridderived populations were not uncommon in coastal and inland northern California Panetsos and Baker 1967 Some 40 years later in a wide sampling of Raphanus throughout the state hybrid genetic ancestry was found for every population Hegde et al 2006 Ridley et al 2008 Thus over the last century the two Raphanus species have coalesced into a hybrid lineage that has displaced all natural populations of both parents Commonly referred to as “California wild radish” this lineage is now found throughout a major portion of naturally disturbed coastal areas and humandisturbed inland sites in California DiTomaso and Healy 2006 Panetsos and Baker 1967 as well as south into Baja California Mexico and north into Oregon Hegde et al 2006 Ridley 2008 Interestingly interspecific Raphanus hybrids also appear in Europe but are not invasive Stace 1975Raphanus is an important model system Plant ecologists evolutionists and geneticists have all used Raphanus for studying pollination biology lifehistory variation ecological genetics floral evolution and plantherbivore interactions eg Campbell et al 2006 Conner 1997 Elam et al 2007 Ellstrand et al 1989 Irwin et al 2003 Marshall and Diggle 2001 Mazer and Schick 1991 Stanton et al 1991Here we use a common garden field experiment to gain evidence for one mechanism by which California wild radish has replaced its progenitors on the western coast of North America Phenotypically California wild radish tends to show intermediacy to its progenitor species for many traits including bolting and flowering dates and root length and width but it exceeds both progenitors for average fruit weight a potential fitness correlate Hegde et al 2006 In addition advanced generation artificial R sativus × R raphanistrum hybrids grown in southern California have shown a significant survival and reproductive advantage over the weedy progenitor R raphanistrum Campbell et al 2006 Given this evidence we hypothesize that the naturally hybridderived California wild radish will show enhanced fitness relative to the species that hybridized to create it and that this could be one mechanism for its successful establishment and spread in the state

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